The Swedish example of food animal production without extensive use of antibiotics – or “healthy animals do not need antibiotics”

Objective To describe how stakeholders at different levels in food animal production in Sweden work to contain antibiotic resistance, with a special focus on poultry production. The stakeholders’ perceptions of antibiotic resistance and awareness of the One Health concept were also studied. Methods This is an interview study with thirteen informants. They represent policymakers, trade organisations, and veterinarians and farmers in the poultry industry. Interview transcripts were analysed using content analysis. The analysis continued until a latent theme emerged, and then the content was rearranged in four domains. Findings A latent theme “Working in unison” emerged, based on the consistency expressed by the informants when they discussed antibiotic resistance, use of antibiotics and food animal production methods. The theme was built on four domains, representing the content of the interviews: Knowledge and engagement; Cooperation; Animal health concept; and Development in balance with economic prerequisites. The work for healthy animals started in Sweden already in the 1920-ies and continued step by step in cooperation and with support from the government. In 1986 Sweden became the first country to ban antibiotics for growth promotion. Veterinarians were considered important drivers of processes by spreading knowledge and working close to the farmers. Farmers felt involved in the development of production methods. The One Health concept was well known among stakeholders working at national level but not among veterinarians in production or farmers. Conclusions Sweden has come far in work to contain antibiotic resistance in the animal sector by practicing restrictive use of antibiotics in food animal production. This practise is based on a long tradition of cooperation among stakeholders, from policymakers to farmers, and with a primary focus on animal health and welfare.

To describe how stakeholders at different levels in food animal production in Sweden work to contain 23 antibiotic resistance, with a special focus on poultry production. The stakeholders' perceptions of 24 antibiotic resistance and awareness of the One Health concept were also studied.

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This is an interview study with thirteen informants. They represent policymakers, trade organisations,

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and veterinarians and farmers in the poultry industry. Interview transcripts were analysed using 28 content analysis. The analysis continued until a latent theme emerged, and then the content was 29 rearranged in four domains.

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A latent theme "Working in unison" emerged, based on the consistency expressed by the informants 32 when they discussed antibiotic resistance, use of antibiotics and food animal production methods. The a "One Health" approach (6). This approach was taken since resistant bacteria can be transmitted 55 between humans, animals, food and the environment, and across international borders. This action 56 plan emphasises a need for coordination among international sectors and actors including human and 57 veterinary medicine, agriculture, environment, finance and consumers (6).

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Efforts to contain antibiotic resistance started early in Sweden. In the human health sector "Strama", 59 the Swedish strategic programme against antibiotic resistance, was formed in 1995 (7). Even earlier, in 60 1986, the use of antibiotics for growth promotion in food producing animals was banned (8). Today

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Sweden has low levels of antibiotic use, and one of the lowest levels of antibiotic resistance compared 62 to most countries in the world (9). The Swedish government strategy for containing antibiotic 63 resistance from 2016 takes a One Health approach (10) with the overall goal to preserve the possibility 64 of effective treatment of bacterial infections in both humans and animals. The strategy was up-dated in one from human sector (human sector study is presented elsewhere). This pilot test did not change the 98 interview guide and these informants were included in the studies.

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The interviews were performed at a place convenient for the informant, often at their workplace. The

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informants could associate and speak freely from the main questions, and the interviewer followed the 101 conversation and asked probing questions. All interviews were audio-recorded and transcribed 102 verbatim by an external transcriber. Before the analysis started, the interviews were listened through 103 and transcripts checked by author IB. The results of the content analysis are presented in Table 3, which shows the relation between theme,   125 domains and categories, followed by a description of each domain and its categories. The descriptions 126 in general represent the whole informant group, and focus primarily on poultry production. When a 127 statement is related to a specific category of informants, the category is given, e.g. the category 128 "veterinarian/s" is used when veterinarians from different categories express a similar perception.

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Descriptions are then followed by table 4, which presents quotes from the informants in the domains.
130 Table 3. The categories are sorted in the domains that were identified together with the latent theme.

Theme Domain Category
Perceptions of antibiotics and antibiotic resistance We must do what we can to contain antibiotic resistance The use of antibiotics must be reduced antibiotics in need of more resources, and that this is a political issue.

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Except for one of the farmers, the informants were very concerned about antibiotic resistance, and 142 described it as a very serious threat. They understood that antibiotic resistance means that we cannot 143 treat diseases, not perform surgery safely, as well as increased mortality. A common perception was 144 that antibiotic resistance already exists, but that the real threat is a future problem. One policymaker 145 informant pointed out the economic consequences of antibiotic resistance and referred to estimates 146 from the World Bank Group. A farmer thought that soon people will hesitate to travel abroad, due to 147 the risk of bringing back antibiotic resistance. Some of the veterinarians compared the antibiotic 148 resistance issue with the issues of environment and climate -creeping threats, and issues which bring 149 out the need for behaviour change in humans. Furthermore, climate change and antibiotic resistance 150 were said to be connected, and climate change can increase the problem of antibiotic resistance.

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Informants perceived antibiotic resistance as caused by too extensive consumption of antibiotics in the 152 human sector, but the animal sector also contributes to the development of antibiotic resistance. They 153 also felt that antibiotic resistance mainly developed abroad and then imported to Sweden.
Veterinarians had comprehensive knowledge and could explain how antibiotic resistance develops.

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Some veterinarians explained that resistant bacteria we bring home when travelling disappear after a 156 while. One policymaker informant asked for more knowledge about how chemicals as heavy metals 157 and biocides can stress bacteria into developing resistance.

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We must do everything possible to contain antibiotic resistance 159 All veterinarians emphasized that we must do what we can to contain antibiotic resistance. In their

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The use of ABs must be reduced

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The veterinarians explained that eradicating antibiotic resistance is difficult but that reducing antibiotic 173 use is possible. The purpose is to reduce selection pressure. The use or non-use of antibiotics in food 174 producing animals is a matter of production methods, veterinarians said.

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Methods to reduce antibiotics in food producing animals were similar to methods in humans, e.g.

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finding alternatives to antibiotics, refraining from antibiotics when treatment is not necessary, and 188

Awareness, knowledge and information is needed
189 The informants expressed that awareness, knowledge and understanding was necessary among

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Cooperation in Sweden between animal and human sectors at policy level has a longstanding history,

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in Strama since the 90s, and later at the Swedish cooperative platform. Here animal and human sectors 216 agree to reduce the antibiotic use. A rather new discussion was cost sharing, meaning that costs were 217 to be shared by both sectors when actions were taken in the animal sector for the sake of public health.

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One hindering factor expressed by the veterinarians was the 'blame game'. This meant blaming other 219 professionals, sectors or other countries for doing less, a belief that others must change but that we are 220 doing enough. This could happen between animal and human sectors, both locally and internationally,

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or when statistics on antibiotic use were presented and countries were compared. Such attitudes could 222 hinder the will to cooperate and stop efforts to reduce antibiotic use. Two policymaker informants knew that antibiotic resistant bacteria can be found in the environment,

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and that the meaning of this is not yet known. They explained that we need more knowledge to 233 understand the meaning and how the environmental sector shall be involved in the One Health work.

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The other informants had no knowledge of antibiotic resistance in the environment but reflected on the 235 issue. 236

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Use of antibiotics to animals in Sweden is low

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All informants talked about how little antibiotics are used in food producing animals in Sweden.

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Antibiotic use was especially low in chicken farming and was not used at all in egg production. Areas

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The informants did not see antibiotic resistance as a problem in food animal production in Sweden.

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The farmers said it did not affect their work. However, all informants talked about the fact that in 2010

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Swedish chickens were infected by ESBL from breeding animals. Despite hard work Swedish 246 chickens may still carry ESBL. As one veterinarian in production explained, E coli infections in 247 chickens are not treated with antibiotics so as not to promote spread of ESBL resistance.

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All informants perceived antibiotics to be extensively used in food producing animals abroad. One  supply. Veterinarians and farmers stated keeping animals' health was a daily never-ending process.

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Chicken production in Sweden was described by the informants as industrial, large-scale and well 292 controlled. Globally, the chicken industry was described as a pyramid, with a few breeding companies 293 on top producing grandparents to all chickens in the world. Sweden buys from two of these breeders.

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There are two levels in Sweden above the chicken farmers, breeders and hatcheries. The hatcheries 295 deliver chickens to the farmers, which in turn are connected to a slaughterhouse. The slaughterhouse 296 does a planning based on peoples' demand of chicken and calculates the number of chickens to be 297 ordered from the hatchery, and when they need to be delivered. After delivery the chickens live 298 indoors until slaughter. Biosecurity was prioritized, and locally produced food was recommended 299 before ecologic production, which was regarded riskier for chickens and too costly for many 300 consumers. This was an overall perception among the informants, except one farmer who had small-301 scale ecological egg production.

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Economy rules food production in Sweden

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Economy rules the chicken production and the production methods. A farmer explained the economic 331 interest to follow all control programs very carefully, especially when you have a large production it 332 will be very costly if something goes wrong. A veterinarian in production reflected that it is not laws 333 that rule production methods, it is profitability. One veterinarian believed that in Sweden, agreements and guidelines had been more important than legislation, while another believed that governmental 335 financing had controlled the development of food production methods and there had been both 336 legislation and voluntary actions. The government has contributed financially to eradication of 337 diseases.

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All informants felt that farmers must be able to live on their production. If they cannot sell their goods, 339 production will cease. Buying Swedish meat supports a production that uses less antibiotics, and not 340 buying Swedish products means moving the antibiotic resistance problem somewhere else. However, 341 production without antibiotics was said to be more expensive and informants suggested that the 342 Swedish government could support Swedish production by explaining to consumers why Swedish 343 meat is more expensive. There was a belief that many Swedish consumers trust the Swedish 344 production of meat.

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Veterinarians expressed that we must safeguard the production we have, and governmental politicians 346 must know this. Threats to the Swedish production were highlighted, for instance too strict 347 regulations, lack of understanding of the factors that can undermine the food industry, and Swedish 348 animal-rights organisations which work hard to eliminate Swedish animal food production.

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Politicians have a responsibility for the antibiotic resistance issue. Regarding this, policymaker 350 informants seemed to think globally and the other informants nationally or at EU level. Politicians 351 need to allocate resources for research, monitoring and education. One farmer was sceptical and felt 352 that politicians think too short-term. Containing antibiotic resistance is politically charged, one trade 353 organisation informant said, reflecting on selling meat in the common market.

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The informants thought it was difficult to assess whether enough resources were allocated to 355 containing antibiotic resistance. Some policymaker informants mentioned that authorities needed more  Table 4. Quotes from the informants sorted in domains. All the informants have contributed to the 370 following quotes.

Domain Quotes
We have two possible tools we can work with -wise antibiotic use, and we can work with preventing infections. And then it is not only the spread of resistant bacteria, but all kinds of infections.
[…] As it looks today, we can't afford not to work with both tools, and I don't believe, I don't believe it will be as effective if we don't work with both.
Policymaker informant 1 So we try, oh, oh…yes…to keep discussions alive during the whole year, both about disease control but above all the use of antibiotics in this area. between different stakeholders in Sweden. The latent theme "Working in unison" was based on the 377 consistency expressed among the informants when they discussed antibiotic resistance, use of 378 antibiotics and production methods, with a special focus on poultry.

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The WHO guidelines for antibiotic use in food-producing animals include complete restriction of 380 antibiotic use for growth promotion and disease prevention in healthy animals, and restrictive use of 381 antibiotics identified as critically important for humans (13). Recommendations are based on evidence

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of decreased presence of bacterial antibiotic resistance in animals, and also humans, after interventions 383 to reduce antibiotic usage (14). According to our findings, the WHO guidelines are followed in

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Sweden. Studies have shown that stakeholders in food production may believe they use less antibiotics 385 than others (15). This could also be the case here. However, statistics on antibiotic use in food 386 producing animals show that antibiotic usage in Sweden is low, only Norway and Island use less 387 antibiotics (9). 388

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Regulations and action plans at global and national levels recommend restrictive antibiotic use in order 390 to contain antibiotic resistance. To make a change, theory needs to be transformed into practice, and 391 actors need to believe in the message. Some actors contest the link between agricultural antibiotic use 392 and antibiotic resistance, but studies report compelling supporting scientific evidence for the need to journey towards lower antibiotic use, it can probably help with a One Health approach. Sweden has 501 worked for 20-30 years to get where it is today. That time does not exist for countries about to start 502 their work now. Hopefully, a strategy based on One Health will help and be more effective. Also, it 503 will be interesting to see how the One Health approach will influence antibiotic resistance containing 504 measurements in Sweden.

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Limitations and strengths 506 Trustworthiness is of major importance in all research. In this study we used the criteria developed by 507 Lincoln and Guba to ensure high quality (37,38). To meet the criteria of credibility we recruited 508 stakeholders with different experience to gain a broad view of perceptions. Furthermore, the analysis 509 was well structured and carefully performed. Quotations from the text are used to demonstrate 510 confirmability. Transferability must be judged by the readers themselves and to make this possible we 511 described how the data were collected and analysed and gave background information about the 512 participants. Due to practical and financial reasons the number of informants was limited. The study 513 included a small number of Swedish stakeholders, and practitioners had experience from poultry 514 sector. The poultry farmers were recruited via the veterinarians, and it is possible that they had more 515 knowledge of antibiotics and were more motivated to work according to guidelines than farmers in 516 general. However, we recruited one egg farmer separately and used this interview to get a wider 517 picture. This informant never used antibiotics on the farm, and awareness of antibiotic resistance was 518 low. Like the other farmers the informant primarily described the daily work to help the animals to 519 stay as healthy as possible. A strength of our study was the choice of personal interviews, which often 520 give richer material, instead of by telephone, which might have produced more interviews.

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Additionally, our findings are in line with the perceived opinion in this field in Sweden and the 522 consistency in responses means we feel that our findings give a good picture of knowledge, attitudes 523 and practices in this sector.

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Sweden has come far in the work to contain antibiotic resistance in the animal sector by practicing 526 restrictive use of antibiotics in food animal production. This practise is based on a long tradition of