Knowledge, attitude and perception regarding antimicrobial resistance

Preventive Veterinary Medicine 156 (2018) 76–83

Contents lists available at ScienceDirect

Preventive Veterinary Medicine journal homepage: www.elsevier.com/locate/prevetmed

Knowledge, attitude and perception regarding antimicrobial resistance and usage among ruminant farmers in Selangor, Malaysia

T

M.B. Sadiqa, S.S. Syed-Hussainb, S.Z. Ramanoona, A.A. Sahareeb, N.I. Ahmadc, M.Z. Noraziahd, ⁎ S.F. Khalida, D.S. Naseehaa, A.A. Syahiraha, R. Mansora, a

Department of Farm and Exotic Animal Medicine and Surgery, Malaysia Department of Veterinary Clinical Studies, Malaysia c Department of Veterinary Pathology & Microbiology, Faculty of Veterinary Medicine, Universiti Putra Malaysia, 43400 UPM Serdang, Malaysia d School of Diagnostic and Applied Health Sciences, Faculty of Health Sciences, Universiti Kebangsaan Malaysia, 50300, Kuala Lumpur, Malaysia b

A R T I C LE I N FO

A B S T R A C T

Keywords: Antimicrobial resistance Antimicrobials Antibiotics Farmers Ruminants

The increasing public health problem of antimicrobial resistance (AMR) has been linked to the extensive antimicrobial use (AMU) in food animals. We conducted a survey among ruminant farmers in Selangor, Malaysia to assess their level of awareness on AMR, attitudes towards AMU, and determinants that influence their practices. The survey was developed in English and Malay, validated, and administered to ruminant farmers in Selangor. A total of 84 farmers (response rate of 55%) completed the structured questionnaire. They appeared to be little aware of AMR and the impact on animals and public health. Indications of inappropriate AMU include their misconception on conditions requiring antibiotic therapy and easy accessibility to antibiotics. More than 70% (60/84) of the respondents believed that all sick animals need to be given antimicrobials. Half of the farmers especially those involved in the production of small and large ruminants; namely mixed ruminant farmers (MRF) (63%, 31/49) indicated that antimicrobials do not have any side effects in animals. Sixty-four percent (54/84) of the farmers have stored antimicrobials in their farms of which the practice was more common (P = 0.02) among the MRF compared to the single ruminant farmers (SRF). Although most of the farmers felt good farm biosecurity will help reduce AMU, they were indifferent regarding using antimicrobials only when prescribed by a veterinarian and non-storage of antimicrobials for later uses. Farmers with larger herd size (> 100 animals/herd) and few years of farming experience agreed more to the suggestions about their role and that of veterinarians respectively in reducing the drivers of AMR. These areas might need to be considered by advisors to inform ruminant farmers on AMR and to encourage them for prudent AMU in food-producing animals.

1. Introduction The emergence of antimicrobial resistance (AMR) in bacterial pathogens is now a threat to the animal and human population in most parts of the world, with potential risks of antimicrobial resistant bacteria transmission from livestock into the environment and food chain (WHO, 2014; Kramer et al., 2017). Livestock production has expanded through intensive farming systems to meet the growing demand for animal products, which is considered to be more efficient and economically practical. However, the aftermath of such growth is the exposure of food animals to antimicrobials used by farmers for different purposes. Antimicrobial usage (AMU) in food-producing animals at therapeutic levels has been suggested to significantly improve the health, productivity, and economic returns by reducing disease incidence, morbidity and mortality of livestock animals (Barlow, 2013).

⁎

Antimicrobials are also increasingly used in livestock for non-therapeutic purposes such as growth promoters and enhancing feed efficiency (Ellerbroek et al., 2010). Nevertheless, these activities could enhance the proliferation of bacteria that are drug-resistant, thus reducing the effectiveness of common drugs used for the treatment of bacterial diseases in food animals (Speksnijder et al., 2015; Wall et al., 2016). Another important concern is the impact of AMU on humans via food supply since the same classes of antimicrobials are used in veterinary and human medicine (Hillerton et al., 2017). Ruminants are important food-producing animals and a major driver of the economy in developing countries. However, they could also pose a threat to human population due to increase exposure to zoonotic pathogens and food-borne diseases (Katakweba et al., 2012). For instance, dairy cattle could act as a reservoir for human pathogens such as Salmonella and Campylobacter, which could transfer genes

Corresponding author at: Department of Farm and Exotic Animal Medicine and Surgery, Faculty of Veterinary Medicine, Universiti Putra Malaysia, 43400 UPM Serdang, Malaysia. E-mail address: [email protected] (R. Mansor).

https://doi.org/10.1016/j.prevetmed.2018.04.013 Received 11 November 2017; Received in revised form 19 April 2018; Accepted 19 April 2018 0167-5877/ © 2018 Elsevier B.V. All rights reserved.


M.B. Sadiq et al.

‘True or False’ responses, while items in the second part were presented using Likert type scale anchored by 1 (strongly disagree) to 5 (strongly agree) (Ary et al., 2010). The demographics of the farmers and management practices were recorded in the last section, which included management system, species of ruminants, purpose of keeping livestock, herd size, age, and years of farming experience. A pilot study was carried out on 11 small ruminant farmers enrolled in a herd health program for Ladang Angkat (Foster Farms) of the Faculty of Veterinary Medicine, Universiti Putra Malaysia, to improve the comprehension and consistency of the items in the questionnaire.

encoding resistance to antibiotics from one bacterium to another (Oliver et al., 2011). Hence, the misuse of antimicrobials either by farmers or veterinarians could potentiate AMR to antibiotics used in animals and humans. At the national level, the less developed countries are more vulnerable to AMR as infectious diseases are common with a huge reliance on antimicrobials for therapeutic purposes (Singh, 2017). In the Malaysian context, ruminants are important in the livestock industry with majority of farmers producing either small or large ruminant for milk and meat products for public consumption (Shanmuganvelu, 2014). Therefore, there is a great concern for food safety and quality in the ruminant sector of the livestock industry. According to the National Pharmaceutical Control Bureau (NPCB), Ministry of Health, Malaysia (2009), AMR is a serious health threat in Malaysia and reducing on-farm AMU in food animal production seems to be the most appropriate intervention in combating the AMR threat originating from animals (Kramer et al., 2017). Lowering the use of veterinary antibiotic to the absolute effective dosage will not only safeguard the animal health but also ensure a sustainable animal production (Speksnijder et al., 2015). Unfortunately, inadequate information on the use of veterinary antibiotics among ruminant livestock in Malaysia might impair our full understanding of the current AMR situation in Malaysian ruminant sector. Selangor is one of the 13 states with the highest population of ruminant farmers in Malaysia (DVS, 2013). However, little is known about farmers' perception on antimicrobials and the usage relating to AMR. Understanding their knowledge and perception on AMR is important, to determine the contributing factors to potential misuse or overuse of antimicrobials in their practice. Consequently, tailored intervention towards ruminant farmers to promote prudent AMU is pertinent in containing AMR threat. Therefore, the objectives of this study were to assess the level of awareness, knowledge, and practices of ruminant farmers on AMR and AMU in Selangor, Malaysia.

2.3. Questionnaire administration The contacts and email address of farmers were obtained from the registry list provided by the DVS, Selangor, Malaysia. A convenience sample of 185 farmers was reached via phone calls and emails to seek for their consent to take part in the survey. The purpose of the study and confidentiality of all information provided was made known. Those willing to participate indicated the preferred means of filling the questionnaire either through online Google form or self-administration and the medium of communication (Malay or English). Thereafter, the online link was sent to 120 farmers, while 34 farmers were visited for self-administration in paper format. Farmers were informed to fill the questionnaire themselves with all the instructions and guidelines well indicated. The questionnaire was administered from June, 2017 to September, 2017. 2.4. Ethical approval

2. Materials and methods

Approval for the study was obtained from the Human Ethics Committee of the Universiti Putra Malaysia (Ref: JKEUPM-2018-003). All the guidelines for the inclusion of human subjects in research were followed and response to the questionnaire constituted the participants’ oral consent.

2.1. Study area and population

2.5. Statistical analysis

The study was carried out in Selangor on the west coast of Peninsular Malaysia, approx. 3°20′N and 101°30′E. All ruminant farmers who are registered with the Selangor state of Department of Veterinary Services (DVS), Malaysia were the target population.

The IBM SPSS (version 23.0) was used in all the statistical analysis. Data from the online Google form was transferred to Microsoft Excel (version, 2010) and copied to SPSS data set, whereas self-administered responses were entered manually into the spreadsheet. The independent variables (age, years of farming experience, farming purpose, educational qualification, and management system) were categorized and assigned with value labels ranging from 0-2 and 0-1 for variables with 3 and 2 levels respectively. The sections for assessing attitude and practices were broadly grouped for SRF and MRF. Descriptive statistics were used to compute median, number of responses and frequency distribution for dichotomous questions. To assess the characteristics of the farmers’ groups (MRF and SRF), a binary logistic regression was applied to investigate their association with the independent variables. First, a univariate analysis was applied and factors significant at P < 0.1 were introduced in the multivariate analysis. Items with dichotomous responses were checked for correlations using the Spearman correlation coefficient. Thereafter, the difference between methods of questionnaire administration and farmers’ responses (dichotomous items) were analyzed using Chi-square test (χ2). The frequency and percentage of respondents given each answer (strongly agree-agree, neutral, and strongly disagree-disagree) on the Likert scale were presented in stacked bar charts. Reliability analysis was used to assess the internal consistency of items in the section and those with Cronbach’s alpha value less than 0.7 were deleted. Categorical principal component analysis (CATPCA) was then conducted to explore the Likert scale responses to each item, identify the structure, and simplify the original variables into components for further analysis. CATPCA is particularly useful in analyzing Likert type variables since it can effectively manage and convert non-linear or

2.2. Instrument and procedure (study design) The developmental stages of the questionnaire entailed a review of the literature related to AMR with emphasis on the factors and practices influencing farmers’ decision on AMU in food-producing animals (Eltayb et al., 2012; Lhermie et al., 2017). To ensure face validity of the questionnaire, practices peculiar to farmers’ in the Malaysia context were also revised. Thereafter, the supposed respondents were categorized into two broad groups; mixed ruminant farmers (MRF) and single ruminant farmers (SRF). The former consisted of farmers engaged in the production of mixed ruminant species (small and large ruminants), whereas the SRF are involved either in small (goats and sheep) or large ruminants (cattle and buffaloes) production. The questionnaire was written in English and Malay languages and developed into four sections. The first section entailed items to assess farmers’ general knowledge on antimicrobials and conditions warranting antibiotics therapy in animals. As a guide, the term antimicrobial was briefly described as “an agent (e.g. antibiotics) that kills or stops the growth of micro-organisms”. Respondents were only required to provide simple responses (e.g. yes or no) or choosing the appropriate answer from multiple choice answers. Farmers’ attitudes toward AMU was investigated in the second section consisting of similar questions demanding ‘Yes’ or ‘No’ responses. Knowledge on AMR was assessed in two parts in the third section. The first being specific statements with 77


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indicated that antibiotics are different from anti-inflammatory drugs and they often adhere to veterinarian’s prescription when administrating antimicrobials to their animals. Sixty respondents (71%) preferred that all sick animals need to be given antimicrobials, while a greater proportion (88%; 74/84) indicated they would follow the instructions on packaged drugs. Also, 22% (19/84) affirmed it is not healthier to administer a less dose of antibiotics rather than the prescribed, whereas only 25% (21/84) felt the need to stop antimicrobial administration once the animal condition improves. Overall, there was no significant difference in the number of farmers from the two categories based on the responses to the aforementioned items. In contrast, the percentage of MRF (40%; 14/35) who believed that some antimicrobials have side effects on livestock were lower (P = 0.02) compared to the SRF (63%; 31/49) (Table 2). When asked if conditions such as diarrhoea, fever, infection of the urinary and respiratory system, ectoparasitic infestations and parasitic gastroenteritis (PGE) warrants antibiotic treatment, more than half of the farmers responded in affirmation (Table 2). The lowest response (58%; 49/84) was for the administration of antibiotics to animals affected with PGE. Between the farmer groups, a higher (p < 0.01) proportion of SRF (76%; 37/49) opted for the need to administer antibiotics to diarrhoeic animals compared with MRF (46%; 16/35) as well as in pyrexia cases (87% vs. 57%, n = 43 vs. 20).

categorical data to quantitative variables via optimal quantification and present data set of a smaller number of dimensions (Linting and van der Kooij, 2012). Component loadings were considered significant if greater or equal to 0.40. Hence, associated variables were regrouped into components, presenting a “loading” depicting the correlation between each original variable and the respective component. Each component was assigned a descriptive summary name, while the component means were computed to assess any relationship with the independent variables. 3. Results 3.1. Characteristics of the study population A total of 84 farmers (55%) participated in the study out of the 154 reached. A higher response rate of 94% (32/34) was obtained from the self-administration format compared with the online survey (43%; 52/ 120). There was no significant difference in the number of responses based on the method of filling the questionnaire. The proportions of SRF and MRF were 58% (49/84) and 42% (35/84) respectively. The median herd size corresponded to those with 50–100 animals/farm (30%; n = 25). Majority of the respondents were less than 50 years old (74%; 62/84) (Table 1). A higher proportion of SRF (57%; 28/49, P = 0.01) have below 10 years of experience compared with MRF (23%; 8/35) in the univariate analysis, whereas a greater proportion of SRF engage in beef (79%; 15/19, P = 0.001) and dairy purpose (87%; 20/23, P = 0.001) compared to MRF (Supplementary Table 1).

3.3. Attitude towards AMU The response of farmers on items regarding attitude towards AMU is shown in Table 3. A greater proportion of respondents (67%; 54/84) stated they have stored antimicrobials in their farms, with a higher (P = 0.02) proportion of MRF (80%; 28/35) affirming such practice compared with the SRF (57%; 28/49). In addition, 31 (37%) farmers stated that their recent AMU was within the last one month. Less than half (46%; 39/84) of the respondents obtained veterinarian prescription prior to the recent antibiotics use with comparable proportions having obtained the antibiotics from animal product suppliers (20%; 17/84) and previous stock (27%; 23/84). Similarly, a higher percentage (73%; 61/84) of farmers indicated that they would not directly sell or slaughter an animal treated with antimicrobials to the market. Excluding the first item regarding antimicrobial storage, there was no significant difference in the responses between the two groups of farmers.

3.2. Knowledge on antimicrobials Forty-four percent (37/84) of the respondents were aware of the term ‘antimicrobials’ prior to this study. More than half of the farmers Table 1 Characteristics of the study population. Variables

Frequency

%

Practice SRF MRF

49 35

58 42

Management system Intensive a Semi-intensive b Mixed c

25 48 11

30 57 13

Purpose of production Beef Dairy Beef and dairy Others d

19 23 35 7

23 27 42 8

Herd size (animals/herd) < 50 50-100 Above 100

28 25 31

33 30 37

Age group (years) < 50 ≥50

62 22

74 26

Educational level Primary and secondary education University education

29 55

35 65

Experience (years) < 10 ≥10

36 48

43 57

3.4. Awareness of AMR Farmers were more aware of the term ‘antibiotic resistance’ and ‘drug resistance’ compared to other terms such as antimicrobial resistance and superbugs (Fig. 1A). The informed farmers majorly attributed their source of awareness to medical personnel (i.e. veterinarians, medical doctor, pharmacist and health workers) followed by family members and friends (Fig. 1B). A higher proportions (above 65%) of the respondents agreed that infections from antibiotic-resistant bacteria might be difficult to treat or could make surgical procedures dangerous. However, farmers were indifferent concerning increasing rate of AMR and its impact on the public, as well as being an important problem in Malaysia livestock industry (Table 4). The response to the items in this section was not significantly different between the two groups of farmers. 3.5. Categorical principal component analysis of farmers’ responses on measures to address the problem of AMR Majority of the respondents (> 60%) agreed to measures such as appropriate AMU in animals and good farm security, while less than half agreed to practices such as non-storage of antimicrobials and reducing AMU in food-producing animals (Fig. 2). The loadings of the Likert type scale variables onto components are presented in Table 5.

SRF = single ruminant farmers, MRF = mixed ruminant farmers. a Animals are housed all year round without pasture grazing. b Animals have access to external pasture grazing all year round. c Animals are housed and given access to external grazing at fixed periods. d Non-commercial purposes. 78


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Table 2 Farmers’ responses (n = 84) to items regarding their knowledge of antimicrobials. Items

Group SRF (%) (n = 49)

MRF (%) (n = 35)

Total (%)

P-value

1. 2. 3. 4. 5. 6. 7. 8. 9. 10. 11.

Part A: General awareness on antimicrobials Have you heard of ‘antimicrobials’ before now? Are AM different from anti-inflammatory drugs? Are AM different from anti-pyretic drugs? Should you follow veterinarian direction when giving AMs to animals? Do every sick animal need to be given AM? Would you give AM according to instruction on the package? Should exposure of AM to sunlight be avoided? Do some AM have adverse effects on animals? Can you consult a veterinarian before AM use in animals? Giving a less dose of AM than the prescribed is healthier? Should you stop AM administration once the animal condition improves?

23 44 36 44 36 42 38 31 35 12 12

(47) (90) (73) (90) (73) (86) (78) (63) (71) (24) (24)

14 (40) 26 (74) 12 (34) 29 (83) 24 (69) 32 (91) 29 (83) 14 (40) 25 (71) 7 (20) 9 (26)

37 70 48 73 60 74 67 45 60 19 21

(44) (83) (57) (87) (71) (88) (80) (54) (71) (23) (25)

0.11 0.93 0.56 0.60 0.67 0.31 0.47 0.02 0.77 0.55 0.91

1. 2. 3. 4. 5. 6. 7.

Part B: Conditions requiring antibiotic therapy Diarrhoea Fever Urinary tract infection Skin infection Respiratory infection Ecto-parasite infestation Parasitic gastro-enteritis

37 43 33 30 33 32 29

(76) (88) (67) (61) (67) (65) (59)

16 20 30 27 28 23 20

53 63 63 57 61 55 49

(63) (75) (75) (68) (73) (65) (58)

> 0.01 > 0.01 0.05 0.17 0.20 0.96 0.85

(46) (57) (86) (77) (80) (66) (57)

Keys: SRF = single ruminant farmers, MRF = mixed ruminant farmers, AM = antimicrobials. Note: Results are presented in the table for ‘Yes’ responses. P-values are computed from Pearson Chi-square statistic (χ 2) between SRF and MRF. *Comparison is within rows and P < 0.05 is significantly different.

Twenty-nine percent of the variation explained by the PCA was the first component extracted. The component was defined as “farmer role”, while the contained variables with loadings greater than 0.4 are as follows; measures of addressing AMR by appropriate AMU, responsibility to administer antibiotics prudently, concern on the impact of AMR on public health, and good farm security. The second component explained 14% of the variation and the variables included the prescription of antimicrobials by veterinarians only when necessary, usage of antimicrobials only when prescribed by a veterinarian, and AMR being one of the major problems in livestock production. This was defined as “veterinarian role”. The third component summarized as “general role” explained 11% of the variation and included veterinarians solving the problem of AMR promptly, farmer assistance in reducing AMR, and administrating fewer antimicrobials to animals by farmers and veterinarians.

A negative correlation was found between component 1 (“farmer role”) and herd size (r = −0.19, P = 0.04), while small but significant positive correlations were observed between component 2 (“veterinarian role”) and years of farming experience (r = 0.20, P = 0.03), and between component 3 (“general role”) and educational qualification (r = 0.21, P = 0.02). Herd size was associated with component 1, as there was a difference (P < 0.05) between the mean values for farmers with herd size less than 50 animals/herd (3.72 ± 1.09) compared with those having 50-100 (4.21 ± 0.66) and above 100 animals/ herd (4.31 ± 0.65). This indicated that the role of farmers in addressing AMR was perceived more important by farmers with higher herd size compared to those with lower herd size. Furthermore, the mean value for component 2 was greater (P = 0.04) for the farmers with ≤10 years (3.80 ± 1.04) compared to those with > 10 years of farming experience (3.31 ± 1.12) (Supplementary Table S4).

Table 3 Farmers’ responses (n = 84) to items relating to their attitude towards antimicrobial use. Items

1. 2.

3. 4.

5. 6. 7. 8. 9.

Group

Do you have AM stored in your farm? When was the last time AM was administrated to your animals? In last one month In last 6 months Last one year Was the last AM use prescribed by a veterinarian? Where was the recent AM sourced from? Animal products suppliers Previous stocks Any advice from a veterinarian prior to administration? Are you aware of proper dosage of AM? Are you aware of specific AM use for certain infections? I will not directly sell or slaughter an animal treated with AM to the public I need an explanation from a veterinarian for any AM prescribed for my animals

P-value

SRF (%) (n = 49)

MRF (%) (n = 35)

28 (57)

28 (80)

54 (67)

0.02

15 (31) 14 (29) 8 (16) 24 (49)

16 (46) 10 (29) 2 (6) 15 (43)

31 24 10 39

(37) (29) (12) (46)

0.53

13 14 23 33 30 35 37

4 (11) 9 (26) 16 (46) 24 (69) 18 (51) 26 (74) 24 (69)

17 23 39 57 48 61 61

(20) (27) (46) (68) (57) (73) (73)

0.30

(27) (29) (47) (67) (61) (71) (76)

Note: SRF = single ruminant farmers, MRF = mixed ruminant farmers, AM = antimicrobials Results are presented in the table for ‘Yes’ responses P-values were computed from Pearson Chi-square statistic (χ 2) between SRF and MRF *Comparison is within rows and P < 0.05 is significantly different. 79

Total (%) (n = 84)

0.57

0.91 0.90 0.37 0.77 0.48


M.B. Sadiq et al.

public awareness of antibiotics use in Putrajaya, Malaysia (Lim and Teh, 2012). The routine practice and use of antibiotics by farmers might influence their relative awareness on antibiotic resistance. Furthermore, medical personnel was the major source of farmers’ awareness on the presented terms, which could arise from interactions with DVS workers and trained personnel engaged in the supply of antibiotics. Although most of the farmers indicated that antibiotics are different from other presented classes of drugs and compliance to the instructions on packaged drugs, the majority of them felt all sick animals needed to be given antimicrobials. Findings such as low awareness and misconceptions concerning AMU amongst livestock keepers were reported in similar studies in Tanzania and China (Chenggang et al., 2011; Katakweba et al., 2012). The emergence of AMR has been associated with under-dosing and prolonged use of antibiotics, thus facilitating the selection and spread of resistant pathogens in animals (Wall et al., 2016). Overall, a majority of the surveyed farmers were little concerned about the impact of AMR on animals and public health. This result is consistent with a study by the EFSA (2015), where only a small fraction of farmers perceived that AMU in food animals constitutes a problem on human health. Also, McDougall et al. (2017) found that farmers had limited knowledge and low concern about the risk of AMR outside their farms. The low awareness amongst farmers on antimicrobials could be due to the fact that issues related to AMR are newly emerging in the Malaysian livestock context. Further, since the surveyed farmers are registered under the DVS, it is expected that majority of them should be aware of AMR. It could be that most of the farmers are not currently assessed by the DVS or information related to AMR is not disseminated to farmers in the region. Veterinarians are charged with the responsibility of making decisions on AMU following disease diagnosis and antimicrobial susceptibility testing. These processes enable the veterinarian to recommend the appropriate treatment regime. Hence, the fact that most farmers in the present study asserted that all sick animals should be treated with antibiotics calls for attention. Malpractices such as inappropriate antibiotics use and wrong doses could be precipitated. Consequently, it was not surprising as the majority of MRF disagreed that some antibiotics could have side effects in animals. Again, they were of the opinion that conditions such as diarrhoea, ectoparasitic infestation, and respiratory infection require antibiotic therapy. In ruminants, conditions such as pneumonia and diarrhoea are major causes of calf mortality (Eshetu, 2014). However, these conditions could be caused by viral and bacterial pathogens (Escherichia coli, Pasteurella and Salmonella spp). These findings indicate that the farmers were unlikely to be practicing AMU responsibly. Factors that could influence such practice include lack of specific knowledge on pathogens causing the diseases, complexities of the number of antimicrobials available for therapeutic purposes, and role of veterinarians in observing AMR on the client’s farms (Reyher et al., 2017). Findings on attitude towards AMU implied that majority of the farmers affirmed they have antimicrobials stored from previous use, while the practice was more common amongst the MRF compared to

Fig. 1. (A) Distribution of farmers based on awareness on AMR related terms (B) Number of farmers and source of awareness.

Therefore, the role of veterinarians in reducing AMR was perceived more important by farmers with less experience (> 10 years) compared with those with higher farming experience.

4. Discussion The characteristics of the study population showed most of the farmers practice semi-intensive management system and less of intensified farming. Constraints such as insufficient land size, housing conditions and the high cost of commercial feeds might explain the low number of intensively managed herds in the state (Shanmuganvelu, 2014). Majority of the respondents were also categorized as MRF compared to SRF. Factors suggestive to influence such practice include lack of available resources to engage in specialized ruminant farming, technical know-how and expectation on investment (Mohd Karim et al., 2014). Accordingly, specialized ruminant farming requires higher levels of intensification and expertise, which might be lacking amongst the farmers in the state. Commercial farmers might conceive the need to produce both large and small ruminants as income from sole practice is not assured. Also, consumers or public demands for various animal food products (beef and milk) might as well contribute to such practice. Although all the farmers understood the meaning of antibiotics, only half of them were aware of the term ‘antimicrobials’ prior to the current study. Again, farmers were more aware of the term ‘antibiotic resistance’ compared to others (AMR and superbugs). The little awareness on the latter terms could be associated with their low educational level. A similar finding was reported in the assessment of Table 4 Farmers’ responses to items regarding their knowledge on AMR.

1. 2. 3. 4. 5. 6. 7.

Items: Which of these is true about AMR

SRF (%)

MRF (%)

Total (%)

P-value

Increasing rate of infections resistant to antimicrobials in animals Infections from antibiotic resistant bacteria could be difficult to treat AMR can greatly affect the animal population AMR is not an issue in Malaysia Antibiotic resistant bacteria can spread from animal to animal Infections from antibiotic resistant bacteria can make surgical procedures dangerous AMR problem in farm animals can cause similar problem in humans

27 40 31 18 29 34 30

20 29 18 18 14 23 21

47 69 49 36 43 57 51

0.85 0.88 0.27 0.18 0.08 0.72 0.91

(55) (82) (63) (37) (59) (69) (61)

Note: SRF = single ruminant farmers, MRF = mixed ruminant farmers, AMR = antimicrobial resistance. Results are presented for ‘True’ responses. P-values were computed from Pearson Chi-square statistic (χ 2). 80

(57) (83) (51) (51) (40) (64) (60)

(56) (82) (58) (43) (51) (68) (61)


M.B. Sadiq et al.

Fig. 2. Distribution of responses (agree, disagree and neutral) among farmers in Selangor (n = 84) based on suggested measures in addressing AMR.

potential drivers of AMR in public health (WHO, 2014). Other indications of potential misuse of antimicrobials as presented by the majority of the surveyed farmers included recent administration of antibiotics to animals without veterinarian prescription and obtaining such drugs either from previous stocks or animal products suppliers. Drug suppliers such as pharmaceutical companies have the financial strength to make antimicrobials available for farmers, while some veterinarians also engage in sales of drugs as a source of income. In Malaysia, veterinarian prescription is necessary before antibiotics licensed by the DVS are obtained by farmers. However, such policies are not fully implemented or lacking in strict enforcement (HAIAP, 2013). Withdrawal times are often recommended in order to prevent the presence of antimicrobials residues in food products (Lhermie et al., 2017). Such withdrawal duration is also legislated by the DVS, Malaysia. Accordingly, a higher proportion (73%; 61/84) of the farmers surveyed opted they will neither sell nor slaughter animals that had been recently treated with antimicrobials to the market. Although we did not assess the reasons for such response, factors such as religious beliefs and policies enacted by the DVS concerning AMU might compel farmers in ensuring safety provisions of animal food products. Nevertheless, the proportion of respondents with a contrary opinion (27%; 23/84) in the present study is important. In a study by Nonga et al.

SRF. Karimuribo et al. (2015) stated that the habit of stocking drugs by livestock farmers could be widespread in less developed countries characterized by suboptimal veterinary facilities. As found in this survey, farmers highlighted that they often store antimicrobials as a last resort due to delay in veterinary services leading to economic loss. Management system and type of production could also influence farmers’ perception and demand for antimicrobials (Schulze-Geisthovel et al., 2016). The system of rearing both large and small ruminants (MRF) especially in intensified systems might require more management input, thereby increasing AMU by farmers. For instance, larger quantities of antibiotic use were reported in professional sheep and goat farms with larger herd size compared with small-scale farms in the Netherlands (Santman-Berends et al., 2014). Another important aspect is farmers’ access to over the counter antibiotics. About 97 different antimicrobials are registered for use under the NPCB, Ministry of Health, Malaysia, and most of the drugs are used in the livestock industry. Example of these drugs include cephalosporins, penicllins, tetracyclines, aminoglycosides, sulfanamides, and macrolides (Mazuki, 2017). Some of the antibiotics fall under the critical important antimicrobials for human health and their use needs to be restricted in veterinary medicine. Hence, availability of these antimicrobials could further potentiate their suboptimal use in the livestock industry as

Table 5 Rotated component matrix showing the loading between individual variables regarding measures of addressing AMR and the components extracted by CATPCA analysis. Variables

Component 1

2

3

Farmers should not store AM for later use in animals Appropriate AMU can reduce the risk of antibiotic resistant bacteria infections in animals AMR problem can be reduced by good farm security I am worried about the impact of AMR on my health and my animal well-being AM should only be administered to animals when prescribed by veterinarians AMR is one amongst the biggest problem in livestock production Veterinarians should only prescribe AM when necessary Famers can help much to stop AMR Veterinary experts will solve the problem of AMR problem promptly Administer AM to animals only when prescribed by a veterinarian

0.846 0.788 0.568 0.497 – – – – – –

– – – – 0.820 0.740 0.533 – – 0.421

– – – – – – – 0.763 0.599 0.574

Ordered values according to the loading onto components Component 1: “farmer role” Component 2: “Veterinarian role” Component 3: “Combined role”

% variance 28.7 14.4 11.2

Cumulative variance 28.7 43.1 54.3

AM = antimicrobials, AMR = antimicrobial resistance, AMU = antimicrobial use. Component loadings < 0.40 are not displayed. 81


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References

(2010) where 90% of the farmers surveyed affirmed to be aware of antibiotics withdrawal period, 95% of them admitted to having slaughtered chickens before the elapse of the withdrawal time. The lower percentage with such attitude in the present study might be attributed to the different purpose of production. Also, farmers in this study felt veterinarians need to explain the reasons for any antimicrobials prescribed for their animals. In order to improve the prudent AMU, veterinarians play a crucial role by communicating effectively to farmers and decision making should be highlighted with brief clarity on the rationale for the antibiotic prescription to the farmer (Reyher et al., 2017). In the present study, farming experience and herd size was associated with “veterinarian role” and “farmer role” respectively in curtailing the drivers of AMR. Accordingly, measures relating to the actions of veterinarians in reducing AMR were little perceived by the more experienced farmers (> 10 years). Farmers tend to accord much value to the knowledge gained through farming experience, which was reported as the next major reason in farmers’ decision making on AMU after veterinarian advice (McDougall et al., 2017). Hence, farmers with vast experience might perceive AMR as little important problem. Contrarily, farmers just verging into ruminant farming might have a different perception, since they relatively lack the habit of perceived behavior common in experienced farmers. Although, veterinarians were the studied unit, Speksnijder et al. (2015) found a negative association between years of practical experience and awareness about the impact and consequences of AMR. On the same note, smaller sized farms (< 50 animals/herd) compared with higher farm size (> 100 animals/herd) disagreed to the suggested measures regarding their role in combating AMR. Additional efforts might be necessary to convince these farmers in adhering to new standards related to AMU in food animals.

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5. Conclusion This is the first study to report the awareness and perception of livestock farmers on AMU and AMR in Malaysia. In conclusion, farmers responding to this survey were little aware of the prudent use of antimicrobials and the impact of AMR on animal and human health. This is well indicated based on their misconception on conditions requiring antibiotics therapy, easy accessibility to antibiotics, and their storage for later uses. It might also require more efforts to convince farmers with more years of experience and smaller herd size on the measures to reduce AMU in animals. Hence, ruminant farmers in the state need to be enlightened and guided on responsible AMU to prevent the development of AMR. Further studies are required to investigate the antibiotics usage and determinants of veterinary antimicrobial prescription in animal husbandry in Malaysia. Funding This study was funded by the Malaysia One Health University Network (MyOHUN), Universiti Putra Malaysia and USAIDS (United States Agency for International Development). Acknowledgements We appreciate the assistance rendered by the Department of Veterinary Services (DVS), Selangor, Malaysia and the farmers for their cooperation to participate in the study. The authors thank all the technical staff of the Department of Farm and Exotic Animal Medicine and Surgery, Faculty of Veterinary Medicine, UPM Serdang Selangor, Malaysia for their assistance in reaching the farmers. Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at https://doi.org/10.1016/j.prevetmed.2018.04.013. 82


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