Zoonoses and Public Health
REVIEW ARTICLE
Introduction to Systematic Reviews in Animal Agriculture and Veterinary Medicine J. M. Sargeant1,2 and A. M. O’Connor3 1 2 3
Centre for Public Health and Zoonoses, University of Guelph, Guelph, ON, Canada Department of Population Medicine, Ontario Veterinary College, University of Guelph, Guelph, ON, Canada Department of Veterinary Diagnostic and Production Animal Medicine, Iowa State University College of Veterinary Medicine, Ames, IA, USA
Impacts
• Systematic reviews are a structured method to synthesize existing • •
knowledge on a topic. Systematic reviews are widely used in a variety of fields, including human healthcare. With some modifications to the methods, systematic reviews are a valuable tool in animal agriculture and veterinary medicine.
Keywords: Systematic review; meta-analysis; narrative review Correspondence: J. M. Sargeant. Ontario Veterinary College, University of Guelph, 103 MacNabb House, Guelph, ON, Canada, N1G 2W1. Tel.: (519) 824 4120, Ext. 54045; Fax: (519) 766 1730; E-mail: [email protected] Received for publication September 5, 2013 doi: 10.1111/zph.12128
Summary This article is the first in a series of six articles related to systematic reviews in animal agriculture and veterinary medicine. In this article, we overview the methodology of systematic reviews and provide a discussion of their use. Systematic reviews differ qualitatively from traditional reviews by explicitly defining a specific review question, employing methods to reduce bias in the selection and inclusion of studies that address the review question (including a systematic and specified search strategy, and selection of studies based on explicit eligibility criteria), an assessment of the risk of bias for included studies and objectively summarizing the results qualitatively or quantitatively (i.e. via meta-analysis). Systematic reviews have been widely used to address human healthcare questions and are increasingly being used in veterinary medicine. Systematic reviews can provide veterinarians and other decision-makers with a scientifically defensible summary of the current state of knowledge on a topic without the need for the end-user to read the vast amount of primary research related to that topic.
Introduction The use of reviews in decision-making In human health care, and increasingly in animal agriculture and veterinary medicine, the evidence-based medicine movement encourages an evidence-based approach to decision-making, whereby the clinician precisely identifies a clinical problem, searches for and critically appraises all relevant information and decides whether or how to use this information. A major challenge to this approach is how to manage the thousands of research results that become available every year. One way to address this challenge is to use reviews of scientific evidence that have been performed by others. The clear advantage for decision-makers is that it is faster and more time efficient than identifying, obtaining and reading all of the relevant primary (i.e. original) research on a topic themselves. Some of the disadvantages © 2014 Blackwell Verlag GmbH Zoonoses and Public Health, 2014, 61, (suppl. 1), 3–9
to using reviews are that they are sometimes not easy to adapt to individual cases, they become outdated as new research is published, the quality of the review itself needs to be addressed, and one can often find conflicting results between reviews (Barnes and Bero, 1998; Hoving et al., 2001). Evaluations of traditional narrative reviews in the medical literature (Mulrow, 1987; McAlister et al., 1999) and on-farm food safety literature (Sargeant et al., 2006b) illustrate that these reviews do not report the use of scientific methods to identify, assess and synthesize the literature available on the review topic, potentially resulting in invalid conclusions. Overview of systematic reviews Well-executed systematic reviews provide a rigorous and replicable method of identifying, evaluating and summarizing 3
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evidence (Cook et al., 1997; Sargeant et al., 2006a). Integral to current definitions of systematic review is the emphasis on employing systematic methods to reduce bias in the identification and evaluation of studies to be included in the review, and a critical appraisal of the risk of bias in the studies included in the review. Therefore, systematic reviews can provide veterinarians and other decision-makers with a scientifically defensible summary of the current state of knowledge on a topic, without the need to read the vast amount of primary research. Systematic reviews address a targeted question or hypothesis using a structured series of steps with multiple reviewers used at several steps to reduce the potential for bias (Fig. 1) (Sargeant et al., 2006a; European Food Safety Authority (EFSA), 2010). A comprehensive and explicit search strategy is used to identify primary studies (i.e. original research) for inclusion in the review, minimizing the potential for selection bias. Selection of studies for inclusion in a systematic review should be based on specific criteria that are applied to abstracts from all citations identified by the search. Data on study characteristics and results are extracted from the primary studies, and risk of bias is assessed for each study. This requires good reporting of study features and results within the primary studies: guidelines are available for human clinical trials (Moher et al., 2010; Schulz et al., 2010) and for trials in large animals and food safety (O’Connor et al., 2010; Sargeant et al., 2010). When a sufficient number of studies with similar outcomes are available, a formal statistical combination of the data from multiple studies (meta-analysis) can be performed. Meta-analysis is an effective way of increasing power and detecting intervention effects where the results in individual studies are unclear or conflicting. This may be
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particularly valuable in animal trials, which may be small and under-powered. When meta-analysis is not possible, qualitative summarization of the available data may still provide valuable input to answer the review question or to identify knowledge gaps. Uses of systematic reviews Systematic reviews have been used increasingly to inform practice and policy in areas ranging from medicine, to education, to public safety. Systematic reviews have been used in health care to address a range of health-related issues such as disease prevalence / incidence, aetiology and risk factors, diagnostic test accuracy and evaluation of preventive or therapeutic interventions (EFSA, 2010). The focus of this article, and other articles in this series, will be on systematic reviews as they pertain to the evaluation of interventions. In this context, ‘intervention’ refers to a treatment used to prevent, reduce or treat an adverse health outcome or event in animal populations and encompasses strategies such as antimicrobials, biologics and dietary or management manipulation. The range of intervention questions that have been answered by systematic reviews includes the following: Does Penicillin reduce the risk of streptococcal throat infections and attacks of rheumatic fever in people who have already had a bout of rheumatic fever? (Manyemba and Mayosi, 2003); Do school-based drug education programs reduce drug use? (McBride, 2003); Do sobriety checkpoints by law enforcement officers reduce the number of alcohol related traffic accidents? (Elder et al., 2003). Similarly, systematic reviews in veterinary medicine have been used to answer a broad range of questions such as What are the best interventions to treat canine atopic dermatitis? (Olivry and Mueller, 2003); What is the efficacy of vaccines for the prevention of pinkeye in cattle? (Burns and O’Connor, 2008); What is the evidence for the effectiveness of acupuncture in veterinary medicine? (Habacher et al., 2006); and What is the evidence for efficacy of selected pre-harvest interventions to reduce faecal shedding of Escherichia coli O157 in ruminants? (Sargeant et al., 2007; Snedeker et al., 2011). Differences Between Systematic Reviews and Traditional Narrative Reviews
Fig. 1. Structured steps used to conduct systematic reviews of the literature (EFSA 2010).
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There is a common but erroneous belief that systematic reviews are the same as traditional narrative reviews, only more comprehensive (Petticrew, 2001). Systematic reviews are not just big literature reviews, and their main objective is not simply to search more databases. Rather, systematic reviews are designed to answer a specific question, to reduce bias in the selection and inclusion of studies, to © 2014 Blackwell Verlag GmbH Zoonoses and Public Health 61 (suppl. 1) (2014) 3–9
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appraise the risk of bias in the included studies and to summarize them objectively. They also differ in the measures taken to reduce bias, for instance using several reviewers working independently to screen papers for inclusion, extract study outcomes and assess the risk of bias in the studies. Even small systematic reviews are likely to involve several reviewers screening thousands of abstracts. As a result, systematic reviews commonly require more time, staff and money than traditional reviews. Systematic reviews are not simply ‘bigger’, they are qualitatively different, as illustrated in Table 1. Systematic Reviews in Human Health Care Historical perspectives Although there are a limited number of written examples, the critical consideration of all scientific research or data on a topic has been an important component of scientific enquiry since the Enlightenment (Hunt, 1997). In many historical examples, attempts were made to synthesize available data or place new data in the context of current knowledge. In a 1904 report published in the British Medical Journal, statistician Karl Pearson synthesized data from several studies on the efficacy of typhoid vaccination. His rationale for pooling data was that ‘Many of the groups. . . are far too small to allow for any definite opinion being formed at all, having regard to size of the probable error involved’ (Pearson, 1904). In the years leading up to and during the Second World War, noted statistician Frank Yates wrote about pooling results from groups of studies using agricultural and livestock examples (Chalmers et al., 2002).
Veterinary Systematic Reviews
Thus, attempts to search for and synthesize evidence to support clinical practice and policy decisions are not new. However, formal approaches and systematic methods for appraising and collating evidence have only been developed in recent decades. This has been in response to calls from the ‘evidence movement’ to organize knowledge into a useable and reliable format (Hansen and Rieper, 2009). Critical appraisal and synthesis of research findings in a systematic manner emerged in the 1970s under the term ‘meta-analysis’ (Chalmers et al., 2002). The phrase was coined by Glass and colleagues who conducted research syntheses to determine the benefits of psychotherapy (Smith and Glass, 1977) and the impact of class size on student achievement (Glass and Smith, 1979). The concept of ‘systematic review’ is newer still and is defined to emphasize the importance of systematic methods to reduce bias in the identification and selection of research results which are to be synthesized through ‘the application of strategies that limit bias in the assembly, critical appraisal and synthesis of all relevant studies on a specific topic’ (Last, 2001). Although initial published syntheses were conducted in the areas of public policy and social interventions, a common early use of systematic research synthesis was in human therapeutics. One important leader in this movement was epidemiologist Archie Cochrane who wrote ‘it is surely a great criticism of our profession that we have not organized a critical summary, by specialty or subspecialty, adapted periodically, of all relevant randomized controlled trials’ (Cochrane, 1979). These influences helped to inform the evidence-based medicine movement of the late twentieth century. Evidence-based medicine has been defined by Sackett et al. (1996) as ‘the conscientious, explicit,
Table 1. Good quality systematic reviews and traditional narrative reviews compared
Review topic – what is the question? Finding data – sources and strategies Selection of studies to include Assessing risk of bias in the included studies Synthesizing study results Inferences
Good quality systematic reviews
Traditional narrative reviews
Clear question to be answered or hypothesis to be tested
Often broad in scope addressing general topics such the epidemiology and or pathology of a disease
Comprehensive search of electronic databases, hand searching of relevant journals, review of references lists and contact with researchers. Explicit search strategy provided including attempts to access unpublished data Explicit description of the types of studies to be included; other criteria specified to limit reviewer bias Formal assessment of the risk of bias in the original research studies is examined in a systematic manner
Not usually specified, often no attempt to find all relevant literature. Therefore, potential for selection bias
Heterogeneity (difference in results) between studies is explicitly described; results are statistically pooled where data and methods are similar Conclusions are based on totality of evidence with a consideration of the risk of bias
Not usually specified. Therefore, potential for selection bias Often do not evaluate risk of bias or differentiate between methodologically sound studies and those with design flaws or potential for biased results Generally no formal statistical pooling of results; Often do not consider differences in study methods or risk of bias in the included studies Conclusions not necessarily based on totality of evidence
Sources: adapted from Cook et al. (1997) and Petticrew (2001).
© 2014 Blackwell Verlag GmbH Zoonoses and Public Health 61 (suppl. 1) (2014) 3–9
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judicious use of current best evidence in making decisions about the care of individual patients’. An important feature of this movement has been the emphasis on research synthesis, with healthcare decision-making based on systematically reviewed and critically appraised research evidence. Benefits of this approach include the ability to balance research evidence collected in a systematic and rigorous manner with the experiences and expertise of stakeholders (Sackett et al., 1996). This applied research approach to practice and policy has contributed to the increasing popularity of structured abstracts and secondary journals summarizing studies of high relevance and methodological quality, the creation of the Cochrane Collaboration and its methodology for systematic reviews, and the publication of texts emphasizing evidence-based decision-making (Guyatt et al., 2004). The principles of evidence-based practice have become core concepts of undergraduate, postgraduate and continuing education in an increasing number of fields including veterinary medicine. Methods for conducting systematic reviews have been designed for the use by those who want to make more informed decisions in clinical practice, healthcare research and public health policy. Examples of groups involved in the methodology and conduct of systematic reviews include the Cochrane Collaboration (www.cochrane.org), the Agency for Healthcare Research and Quality (www.ahrq. gov) and The Centre for Reviews and Dissemination (http://www.york.ac.uk/inst/crd/index.htm). Although there are some differences in the style and focus of these groups, the basic methodological components of their systematic reviews are the same. The websites for these organizations provide detailed guidance documents. Key organizations for human healthcare systematic reviews The Cochrane Collaboration opened its centre in Oxford in 1992 and is now an international network of researchers, academics, practitioners and users committed to the principles of managing healthcare knowledge in such a way that it is quality assured, accessible and cumulative. As of September 2012, the Cochrane Library includes the Cochrane Central Register of Controlled Trials, which now includes more than 680 000 trials, and the Cochrane Database of Systematic Reviews, which currently contains more than 7500 complete Cochrane systematic reviews (Cochrane Collaboration, 2013). The Cochrane Library (including protocols and full reviews) is freely and publically available in many countries. Structured abstracts for all Cochrane reviews are available free of charge to anyone with Internet access. The systematic review format developed and used by the Cochrane Collaboration is internationally recognized as the gold standard for systematic reviews of the 6
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effects of healthcare intervention studies. A handbook describing the process of preparing and maintaining Cochrane systematic reviews is available online (Higgins and Green, 2011). The Agency for Healthcare Research and Quality (AHRQ) is the health services research arm of the United States Department of Health and Human Services, complementing the biomedical research mission of its sister agency, the National Institutes of Health. AHRQ is home to research centres that specialize in major areas of healthcare research such as quality improvement and patient safety, outcomes and effectiveness of care, clinical practice and technology assessment, and healthcare organization and delivery systems. This agency provides research support and policy guidance in health services research and systematic reviews. The Centre for Reviews and Dissemination (CRD) is part of the United Kingdom’s National Institute for Health Research (NIHR) and is a department of the University of York. Established in 1994, CRD is one of the largest groups in the world engaged exclusively in evidence synthesis in the health field. The centre comprises experienced health researchers, medical information specialists, health economists and a knowledge dissemination team. In addition to producing a large range of systematic reviews, CRD also produces internationally accepted guidelines for the conduct of systematic reviews. Systematic Reviews in Animal Agriculture and Veterinary Medicine Systematic reviews are beginning to be used in veterinary medicine and food safety for companion animals, food animals and wildlife, with several hundred systematic reviews on animal health topics published between 2000 and 2013 (a database that includes systematic reviews in veterinary medicine is available at: http://webapps.nottingham.ac.uk/ refbase/). The findings of systematic reviews can offer valuable information on whether interventions are efficacious, compare the efficacy between interventions or can provide data as input into risk assessment models. For instance, a systematic review of multiple pharmacological interventions for canine atopic dermatitis reported good evidence for recommending the use of oral glucocorticoids and cyclosporine, fair evidence for topical triamcinolone spray, topical tacrolimus lotion, oral pentoxifylline or oral misoprostol and insufficient evidence for or against several other interventions including type-1 histamine receptor antagonists, tricyclic antidepressants and cyproheptadine (Olivry and Mueller, 2003). This review also concluded that there was fair evidence against recommending the use of other interventions. © 2014 Blackwell Verlag GmbH Zoonoses and Public Health 61 (suppl. 1) (2014) 3–9
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Systematic reviews can also highlight areas where there is insufficient evidence to assess the efficacy of interventions or where there are common methodological flaws in the available research, thereby providing direction and impetus for future basic and applied research in a specific area. For instance, a systematic review of surgical interventions for canine cranial cruciate ligament injury concluded that none of the surgical procedures evaluated in the review had sufficient data available in the literature to support them giving a consistent return of dogs to normal function (Aragon and Budsberg, 2005). In a systematic review of on-farm interventions to reduce faecal shedding of E. coli O157 in domestic ruminants, several of the interventions considered had only been evaluated using small scale field trials, in many cases using an artificial disease challenge (Sargeant et al., 2007). While the findings provide useful preliminary evidence that an intervention may work, they do not provide strong evidence that the intervention will work under real-life conditions. The same review noted that there were methodological flaws in several of the publications, including failure to report randomization to intervention groups in clinical trials. Thus, systematic reviews can identify knowledge gaps to target needed research and can also identify methodological issues that need to be considered when reading the existing literature and addressed when designing additional primary research studies. However, although the methods for developing systematic reviews of interventions in human health care are well developed, these methods may not be directly applicable to evaluate issues in animal agriculture and veterinary medicine (Sargeant et al., 2006a). An obvious difference between human health care and animal sciences is that animal studies encompass multiple species, and extrapolating results of studies from one species to another may not be appropriate. There are also important differences between human and veterinary medicine in the study designs used to address clinical questions. Randomized controlled trials (RCTs) provide the highest level of evidence for evaluating efficacy of interventions under real-world conditions (Higgins and Green, 2011) and are therefore preferred for inclusion in systematic reviews in both human and veterinary medicine. In human medicine, when a sufficient number of RCTs exist on a topic, systematic reviews of interventions often are restricted to include only results from RCTs. However, there are comparatively few RCTs published in veterinary medicine compared with human medicine, and therefore, observational studies are commonly used, particularly for interventions related to management practices. Additionally, challenge studies, where the investigator controls both the allocation to intervention and the disease occurrence (e.g. by deliberately challenging all study subjects with an infectious disease agent of interest and then randomly allocating study subjects to intervention groups), are often conducted in vet© 2014 Blackwell Verlag GmbH Zoonoses and Public Health 61 (suppl. 1) (2014) 3–9
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erinary research but are generally not used in human healthcare. Animal models of non-infectious diseases can be developed and used in the species of interest in veterinary medicine to evaluate potential interventions. In human medicine, studies using animal models can provide proof of concept for an intervention, but are not included in systematic reviews to evaluate real-world efficacy in humans. In human health care, patients are recruited for a study based on specified eligibility criteria and, with the exception of studies involving children or individuals with cognitive disabilities, provide informed consent for their own participation. In veterinary medicine, animal owners’/care-givers’ consent to participation on behalf of the animals that actually participate in the trial. This means that, in veterinary studies, there often are two ‘levels’ of selection and eligibility: that of the owner and that of the animal subjects. This may have implications for the comparability of trials evaluating the same intervention. There are additional factors to consider when conducting systematic reviews related to livestock species. Agricultural and husbandry practices vary substantively between countries, and livestock generally passes through distinct production stages during their lives which may involve very different dietary, housing and other management practices. Livestock populations are grouped and housed differently from human populations, meaning that aspects of trial design and analyses may differ between trials in livestock species and human trials. Research studies in livestock, particularly clinical trials, may be performed with individual animal intervention allocation and housing (often using an artificial disease challenge), small group intervention allocation and housing, or under typical commercial (field) conditions. When animals are housed in groups, the outcome may be determined based on group level variables, measurements on all animals within the group or subsampling of individuals within the group. Each of these methodological approaches will be associated with different statistical analyses. Therefore, when conducting systematic reviews of livestock-related questions, differences in study designs between studies addressing the same basic question will need to be considered when summarizing and interpreting results from multiple studies. Finally, human medical decisions are made based on the combination of scientific evidence about efficacy of the intervention, the balance of benefits and harms, and patient values and preferences. For livestock species, the balance of benefits and harms to the animal is important. However, there may be additional considerations, such as the costbenefit associated with the use of an intervention, food safety or animal welfare considerations, the producer or owner’s values and preferences, and for some issues the consumer’s values and preferences. Therefore, it is necessary to modify the existing protocols used for systematic 7
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reviews in the human healthcare field for use in systematically evaluating animal research. Despite these challenges, systematic reviews in animal agriculture and veterinary medicine will allow researchers to synthesize the current body of knowledge on targeted issues and lend increased credibility to findings in the field. Conclusion Systematic review is a structured method that has been widely used in human health care to summarize knowledge about the efficacy of interventions. The use of systematic reviews in animal agriculture and veterinary medicine is more recent, and there are difference between human and animal research that need to be considered. However, systematic reviews increasingly are being used in animal agriculture and veterinary medicine and offer an evidencebased method of summarizing primary research. Further articles in this series will overview study design issues when conducting systematic reviews, as well as providing details for each step of the systematic review process. Acknowledgements The authors thank Annette Wilkins for assistance with this manuscript. Funding and in-kind support was obtained from the Laboratory for Foodborne Zoonoses, Public Health Agency of Canada and the Canadian Institutes of Health Research (CIHR) Institute of Population and Public Health/Public Health Agency of Canada Applied Public Health Chair awarded to JM Sargeant. References Aragon, C. L., and S. C. Budsberg, 2005: Applications of evidence-based medicine: cranial cruciate ligament injury repair in the dog. Vet. Surg. 34, 93–98. Barnes, D. E., and L. A. Bero, 1998: Why review articles on the health effects of passive smoking reach different conclusions. JAMA 279, 1566–1570. Burns, M. J., and A. M. O’Connor, 2008: Assessment of methodological quality and sources of variation in the magnitude of vaccine efficacy: a systematic review of studies from 1960 to 2005 reporting immunization with Moraxella bovis vaccines in young cattle. Vaccine 26, 144–152. Chalmers, I., L. V. Hedges, and H. Cooper, 2002: A brief history of research synthesis. Eval. Health Prof. 25, 12–37. Cochrane, A. L., 1979: 1931–1971: A Critical Review, with Particular Reference to the Medical Profession. Medicines for the Year 2000, pp. 1–12. Office of Health Economics, London, UK. Cochrane Collaboration, 2013: The Cochrane Library. Available at: http://www.cochrane.org/tags/tags/cochrane-library (accessed on 14 April 2014).
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Cook, D. J., C. D. Mulrow, and R. B. Haynes, 1997: Systematic reviews: synthesis of best evidence for clinical decisions. Ann. Intern. Med. 126, 376–380. Elder, R., R. Shults, and D. Sleet, 2003: Effectiveness of sobriety checkpoints for reducing alcohol-involved crashes. Traffic Inj. Prev. 3, 266–274. European Food Safety Authority (EFSA), 2010: Application of systematic review methodology to food and feed safety assessments to support decision making. EFSA J. 8, 1637. Glass, G. V., and M. L. Smith, 1979: Meta-analysis of research on class size and achievement. Educ. Eval. Policy Anal. 1, 2–16. Guyatt, G., D. Cook, and B. Haynes, 2004: Evidence based medicine has come a long way. BMJ 329, 990–991. Habacher, G., M. H. Pittler, and E. Ernst, 2006: Effectiveness of acupuncture in veterinary medicine: systematic review. J. Vet. Intern. Med. 20, 480–488. Hansen, H. F., and O. Rieper, 2009: The evidence movement: the development and consequences of methodologies in review practices. Evaluation 15, 141–163. Higgins, J. P. T., and S. Green, 2011: Cochrane Handbook for Systematic Reviews of Interventions Version 5.1. 0 [updated March 2011]. The Cochrane Collaboration. Hoving, J. L., A. R. Gross, D. Gasner, T. Kay, C. Kennedy, M. A. Hondras, T. Haines, and L. M. Bouter, 2001: A critical appraisal of review articles on the effectiveness of conservative treatment for neck pain. Spine (Phila Pa 1976), 26, 196–205. Hunt, M. M., 1997: How Science Takes Stock: The Story of Meta-Analysis. Russell Sage Foundation, New York, NY. Last, J. M., 2001: A Dictionary of Epidemiology. 4th edn, p. 176. Oxford University Press Inc., New York, NU. Manyemba, J., and B. M. Mayosi, 2003: Intramuscular penicillin is more effective than oral penicillin in secondary prevention of rheumatic fever–a systematic review. S. Afr. Med. J. 93, 212–218. McAlister, F. A., H. D. Clark, C. van Walraven, S. E. Straus, F. M. E. Lawson, D. Moher, and C. D. Mulrow, 1999: The medical review article revisited: has the science improved? Ann. Intern. Med. 131, 947–951. McBride, N., 2003: A systematic review of school drug education. Health Educ. Res. 18, 729–742. Moher, D., S. Hopewll, K. F. Schulz, V. Montori, P. C. Gotzsche, P. J. Devereaux, D. Elbourne, M. Egger, and D. G. Altman, 2010: CONSORT 2010 Explanation and Elaboration: updated guidelines for reporting parallel group randomised trials. J. Clin. Epidemiol. 63, e1–e37. Mulrow, C. D., 1987: The medical review article: state of the science. Ann. Intern. Med. 106, 485–488. O’Connor, A. M., J. M. Sargeant, I. A. Gardner, J. S. Dickson, M. E. Torrence, C. E. Dewey, I. R. Dohoo, R. B. Evans, J. T. Gray, M. Greiner, G. Keefe, S. L. Lefebvre, P. S. Morley, A. Ramirez, W. Sischo, D. R. Smith, K. Snedeker, J. Sofos, M. P. Ward, and R. Wills, 2010: The REFLECT Statement: methods and processes of creating reporting guidelines for Randomized Controlled Trials for livestock and food safety by modify-
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ing the CONSORT Statement. Zoonoses Public Health 57, 95– 104. Olivry, T., and R. S. Mueller, 2003: Evidence-based veterinary dermatology: a systematic review of the pharmacotherapy of canine atopic dermatitis. Vet. Dermatol. 14, 121–146. Pearson, K., 1904: Report on certain enteric fever inoculation statistics. BMJ 2, 1243–1246. Petticrew, M., 2001: Systematic reviews from astronomy to zoology: myths and misconceptions. BMJ 322, 98–101. Sackett, D. L., W. M. Rosenberg, J. A. Gray, R. B. Haynes, and W. S. Richardson, 1996: Evidence based medicine: what it is and what it isn’t. BMJ 312, 71–72. Sargeant, J. M., A. Rajic, S. Read, and A. Ohlsson, 2006a: The process of systematic review and its application in agri-food public-health. Prev. Vet. Med. 75, 141–151. Sargeant, J. M., M. E. Torrence, A. Rajic, A. M. O’Connor, and J. Williams, 2006b: Methodological quality assessment of review articles evaluating interventions to improve microbial food safety. Foodborne. Pathog. Dis. 3, 447–456. Sargeant, J. M., M. R. Amezcua, A. Rajic, and L. Waddell, 2007: Pre-harvest interventions to reduce the shedding of E. coli
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O157 in the faeces of weaned domestic ruminants: a systematic review. Zoonoses Public Health 54, 260–277. Sargeant, J. M., A. M. O’Connor, I. A. Gardner, J. S. Dickson, M. E. Torrence, and consensus meeting participants: I. R. Dohoo, S. L. Lefebvre, P. S. Morley, A. Ramirez, K. Snedeker, 2010: The REFLECT statement: reporting guidelines for randomized controlled trials in livestock and food safety: explanation and elaboration. Zoonoses Public Health 57, 105–136. Schulz, K. F., D. G. Alman, D. Moher, and for the CONSORT group, 2010: CONSORT 2010 Statement: Updated guidelines for reporting parallel group randomized trials. J. Clin. Epidemiol. 63, 834–840. Smith, M. L., and G. V. Glass, 1977: Meta-analysis of psychotherapy outcome studies. Am. Psychol. 32, 752–760. Snedeker, K. G., M. Campbell, and J. M. Sargeant, 2011: A systematic review of vaccinations to reduce the shedding of E. coli O157 in the feces of domestic ruminants. Zoonoses Public Health 59, 126–138.
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REVIEW ARTICLE
Introduction to Systematic Reviews in Animal Agriculture and Veterinary Medicine J. M. Sargeant1,2 and A. M. O’Connor3 1 2 3
Centre for Public Health and Zoonoses, University of Guelph, Guelph, ON, Canada Department of Population Medicine, Ontario Veterinary College, University of Guelph, Guelph, ON, Canada Department of Veterinary Diagnostic and Production Animal Medicine, Iowa State University College of Veterinary Medicine, Ames, IA, USA
Impacts
• Systematic reviews are a structured method to synthesize existing • •
knowledge on a topic. Systematic reviews are widely used in a variety of fields, including human healthcare. With some modifications to the methods, systematic reviews are a valuable tool in animal agriculture and veterinary medicine.
Keywords: Systematic review; meta-analysis; narrative review Correspondence: J. M. Sargeant. Ontario Veterinary College, University of Guelph, 103 MacNabb House, Guelph, ON, Canada, N1G 2W1. Tel.: (519) 824 4120, Ext. 54045; Fax: (519) 766 1730; E-mail: [email protected] Received for publication September 5, 2013 doi: 10.1111/zph.12128
Summary This article is the first in a series of six articles related to systematic reviews in animal agriculture and veterinary medicine. In this article, we overview the methodology of systematic reviews and provide a discussion of their use. Systematic reviews differ qualitatively from traditional reviews by explicitly defining a specific review question, employing methods to reduce bias in the selection and inclusion of studies that address the review question (including a systematic and specified search strategy, and selection of studies based on explicit eligibility criteria), an assessment of the risk of bias for included studies and objectively summarizing the results qualitatively or quantitatively (i.e. via meta-analysis). Systematic reviews have been widely used to address human healthcare questions and are increasingly being used in veterinary medicine. Systematic reviews can provide veterinarians and other decision-makers with a scientifically defensible summary of the current state of knowledge on a topic without the need for the end-user to read the vast amount of primary research related to that topic.
Introduction The use of reviews in decision-making In human health care, and increasingly in animal agriculture and veterinary medicine, the evidence-based medicine movement encourages an evidence-based approach to decision-making, whereby the clinician precisely identifies a clinical problem, searches for and critically appraises all relevant information and decides whether or how to use this information. A major challenge to this approach is how to manage the thousands of research results that become available every year. One way to address this challenge is to use reviews of scientific evidence that have been performed by others. The clear advantage for decision-makers is that it is faster and more time efficient than identifying, obtaining and reading all of the relevant primary (i.e. original) research on a topic themselves. Some of the disadvantages © 2014 Blackwell Verlag GmbH Zoonoses and Public Health, 2014, 61, (suppl. 1), 3–9
to using reviews are that they are sometimes not easy to adapt to individual cases, they become outdated as new research is published, the quality of the review itself needs to be addressed, and one can often find conflicting results between reviews (Barnes and Bero, 1998; Hoving et al., 2001). Evaluations of traditional narrative reviews in the medical literature (Mulrow, 1987; McAlister et al., 1999) and on-farm food safety literature (Sargeant et al., 2006b) illustrate that these reviews do not report the use of scientific methods to identify, assess and synthesize the literature available on the review topic, potentially resulting in invalid conclusions. Overview of systematic reviews Well-executed systematic reviews provide a rigorous and replicable method of identifying, evaluating and summarizing 3
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evidence (Cook et al., 1997; Sargeant et al., 2006a). Integral to current definitions of systematic review is the emphasis on employing systematic methods to reduce bias in the identification and evaluation of studies to be included in the review, and a critical appraisal of the risk of bias in the studies included in the review. Therefore, systematic reviews can provide veterinarians and other decision-makers with a scientifically defensible summary of the current state of knowledge on a topic, without the need to read the vast amount of primary research. Systematic reviews address a targeted question or hypothesis using a structured series of steps with multiple reviewers used at several steps to reduce the potential for bias (Fig. 1) (Sargeant et al., 2006a; European Food Safety Authority (EFSA), 2010). A comprehensive and explicit search strategy is used to identify primary studies (i.e. original research) for inclusion in the review, minimizing the potential for selection bias. Selection of studies for inclusion in a systematic review should be based on specific criteria that are applied to abstracts from all citations identified by the search. Data on study characteristics and results are extracted from the primary studies, and risk of bias is assessed for each study. This requires good reporting of study features and results within the primary studies: guidelines are available for human clinical trials (Moher et al., 2010; Schulz et al., 2010) and for trials in large animals and food safety (O’Connor et al., 2010; Sargeant et al., 2010). When a sufficient number of studies with similar outcomes are available, a formal statistical combination of the data from multiple studies (meta-analysis) can be performed. Meta-analysis is an effective way of increasing power and detecting intervention effects where the results in individual studies are unclear or conflicting. This may be
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particularly valuable in animal trials, which may be small and under-powered. When meta-analysis is not possible, qualitative summarization of the available data may still provide valuable input to answer the review question or to identify knowledge gaps. Uses of systematic reviews Systematic reviews have been used increasingly to inform practice and policy in areas ranging from medicine, to education, to public safety. Systematic reviews have been used in health care to address a range of health-related issues such as disease prevalence / incidence, aetiology and risk factors, diagnostic test accuracy and evaluation of preventive or therapeutic interventions (EFSA, 2010). The focus of this article, and other articles in this series, will be on systematic reviews as they pertain to the evaluation of interventions. In this context, ‘intervention’ refers to a treatment used to prevent, reduce or treat an adverse health outcome or event in animal populations and encompasses strategies such as antimicrobials, biologics and dietary or management manipulation. The range of intervention questions that have been answered by systematic reviews includes the following: Does Penicillin reduce the risk of streptococcal throat infections and attacks of rheumatic fever in people who have already had a bout of rheumatic fever? (Manyemba and Mayosi, 2003); Do school-based drug education programs reduce drug use? (McBride, 2003); Do sobriety checkpoints by law enforcement officers reduce the number of alcohol related traffic accidents? (Elder et al., 2003). Similarly, systematic reviews in veterinary medicine have been used to answer a broad range of questions such as What are the best interventions to treat canine atopic dermatitis? (Olivry and Mueller, 2003); What is the efficacy of vaccines for the prevention of pinkeye in cattle? (Burns and O’Connor, 2008); What is the evidence for the effectiveness of acupuncture in veterinary medicine? (Habacher et al., 2006); and What is the evidence for efficacy of selected pre-harvest interventions to reduce faecal shedding of Escherichia coli O157 in ruminants? (Sargeant et al., 2007; Snedeker et al., 2011). Differences Between Systematic Reviews and Traditional Narrative Reviews
Fig. 1. Structured steps used to conduct systematic reviews of the literature (EFSA 2010).
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There is a common but erroneous belief that systematic reviews are the same as traditional narrative reviews, only more comprehensive (Petticrew, 2001). Systematic reviews are not just big literature reviews, and their main objective is not simply to search more databases. Rather, systematic reviews are designed to answer a specific question, to reduce bias in the selection and inclusion of studies, to © 2014 Blackwell Verlag GmbH Zoonoses and Public Health 61 (suppl. 1) (2014) 3–9
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appraise the risk of bias in the included studies and to summarize them objectively. They also differ in the measures taken to reduce bias, for instance using several reviewers working independently to screen papers for inclusion, extract study outcomes and assess the risk of bias in the studies. Even small systematic reviews are likely to involve several reviewers screening thousands of abstracts. As a result, systematic reviews commonly require more time, staff and money than traditional reviews. Systematic reviews are not simply ‘bigger’, they are qualitatively different, as illustrated in Table 1. Systematic Reviews in Human Health Care Historical perspectives Although there are a limited number of written examples, the critical consideration of all scientific research or data on a topic has been an important component of scientific enquiry since the Enlightenment (Hunt, 1997). In many historical examples, attempts were made to synthesize available data or place new data in the context of current knowledge. In a 1904 report published in the British Medical Journal, statistician Karl Pearson synthesized data from several studies on the efficacy of typhoid vaccination. His rationale for pooling data was that ‘Many of the groups. . . are far too small to allow for any definite opinion being formed at all, having regard to size of the probable error involved’ (Pearson, 1904). In the years leading up to and during the Second World War, noted statistician Frank Yates wrote about pooling results from groups of studies using agricultural and livestock examples (Chalmers et al., 2002).
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Thus, attempts to search for and synthesize evidence to support clinical practice and policy decisions are not new. However, formal approaches and systematic methods for appraising and collating evidence have only been developed in recent decades. This has been in response to calls from the ‘evidence movement’ to organize knowledge into a useable and reliable format (Hansen and Rieper, 2009). Critical appraisal and synthesis of research findings in a systematic manner emerged in the 1970s under the term ‘meta-analysis’ (Chalmers et al., 2002). The phrase was coined by Glass and colleagues who conducted research syntheses to determine the benefits of psychotherapy (Smith and Glass, 1977) and the impact of class size on student achievement (Glass and Smith, 1979). The concept of ‘systematic review’ is newer still and is defined to emphasize the importance of systematic methods to reduce bias in the identification and selection of research results which are to be synthesized through ‘the application of strategies that limit bias in the assembly, critical appraisal and synthesis of all relevant studies on a specific topic’ (Last, 2001). Although initial published syntheses were conducted in the areas of public policy and social interventions, a common early use of systematic research synthesis was in human therapeutics. One important leader in this movement was epidemiologist Archie Cochrane who wrote ‘it is surely a great criticism of our profession that we have not organized a critical summary, by specialty or subspecialty, adapted periodically, of all relevant randomized controlled trials’ (Cochrane, 1979). These influences helped to inform the evidence-based medicine movement of the late twentieth century. Evidence-based medicine has been defined by Sackett et al. (1996) as ‘the conscientious, explicit,
Table 1. Good quality systematic reviews and traditional narrative reviews compared
Review topic – what is the question? Finding data – sources and strategies Selection of studies to include Assessing risk of bias in the included studies Synthesizing study results Inferences
Good quality systematic reviews
Traditional narrative reviews
Clear question to be answered or hypothesis to be tested
Often broad in scope addressing general topics such the epidemiology and or pathology of a disease
Comprehensive search of electronic databases, hand searching of relevant journals, review of references lists and contact with researchers. Explicit search strategy provided including attempts to access unpublished data Explicit description of the types of studies to be included; other criteria specified to limit reviewer bias Formal assessment of the risk of bias in the original research studies is examined in a systematic manner
Not usually specified, often no attempt to find all relevant literature. Therefore, potential for selection bias
Heterogeneity (difference in results) between studies is explicitly described; results are statistically pooled where data and methods are similar Conclusions are based on totality of evidence with a consideration of the risk of bias
Not usually specified. Therefore, potential for selection bias Often do not evaluate risk of bias or differentiate between methodologically sound studies and those with design flaws or potential for biased results Generally no formal statistical pooling of results; Often do not consider differences in study methods or risk of bias in the included studies Conclusions not necessarily based on totality of evidence
Sources: adapted from Cook et al. (1997) and Petticrew (2001).
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judicious use of current best evidence in making decisions about the care of individual patients’. An important feature of this movement has been the emphasis on research synthesis, with healthcare decision-making based on systematically reviewed and critically appraised research evidence. Benefits of this approach include the ability to balance research evidence collected in a systematic and rigorous manner with the experiences and expertise of stakeholders (Sackett et al., 1996). This applied research approach to practice and policy has contributed to the increasing popularity of structured abstracts and secondary journals summarizing studies of high relevance and methodological quality, the creation of the Cochrane Collaboration and its methodology for systematic reviews, and the publication of texts emphasizing evidence-based decision-making (Guyatt et al., 2004). The principles of evidence-based practice have become core concepts of undergraduate, postgraduate and continuing education in an increasing number of fields including veterinary medicine. Methods for conducting systematic reviews have been designed for the use by those who want to make more informed decisions in clinical practice, healthcare research and public health policy. Examples of groups involved in the methodology and conduct of systematic reviews include the Cochrane Collaboration (www.cochrane.org), the Agency for Healthcare Research and Quality (www.ahrq. gov) and The Centre for Reviews and Dissemination (http://www.york.ac.uk/inst/crd/index.htm). Although there are some differences in the style and focus of these groups, the basic methodological components of their systematic reviews are the same. The websites for these organizations provide detailed guidance documents. Key organizations for human healthcare systematic reviews The Cochrane Collaboration opened its centre in Oxford in 1992 and is now an international network of researchers, academics, practitioners and users committed to the principles of managing healthcare knowledge in such a way that it is quality assured, accessible and cumulative. As of September 2012, the Cochrane Library includes the Cochrane Central Register of Controlled Trials, which now includes more than 680 000 trials, and the Cochrane Database of Systematic Reviews, which currently contains more than 7500 complete Cochrane systematic reviews (Cochrane Collaboration, 2013). The Cochrane Library (including protocols and full reviews) is freely and publically available in many countries. Structured abstracts for all Cochrane reviews are available free of charge to anyone with Internet access. The systematic review format developed and used by the Cochrane Collaboration is internationally recognized as the gold standard for systematic reviews of the 6
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effects of healthcare intervention studies. A handbook describing the process of preparing and maintaining Cochrane systematic reviews is available online (Higgins and Green, 2011). The Agency for Healthcare Research and Quality (AHRQ) is the health services research arm of the United States Department of Health and Human Services, complementing the biomedical research mission of its sister agency, the National Institutes of Health. AHRQ is home to research centres that specialize in major areas of healthcare research such as quality improvement and patient safety, outcomes and effectiveness of care, clinical practice and technology assessment, and healthcare organization and delivery systems. This agency provides research support and policy guidance in health services research and systematic reviews. The Centre for Reviews and Dissemination (CRD) is part of the United Kingdom’s National Institute for Health Research (NIHR) and is a department of the University of York. Established in 1994, CRD is one of the largest groups in the world engaged exclusively in evidence synthesis in the health field. The centre comprises experienced health researchers, medical information specialists, health economists and a knowledge dissemination team. In addition to producing a large range of systematic reviews, CRD also produces internationally accepted guidelines for the conduct of systematic reviews. Systematic Reviews in Animal Agriculture and Veterinary Medicine Systematic reviews are beginning to be used in veterinary medicine and food safety for companion animals, food animals and wildlife, with several hundred systematic reviews on animal health topics published between 2000 and 2013 (a database that includes systematic reviews in veterinary medicine is available at: http://webapps.nottingham.ac.uk/ refbase/). The findings of systematic reviews can offer valuable information on whether interventions are efficacious, compare the efficacy between interventions or can provide data as input into risk assessment models. For instance, a systematic review of multiple pharmacological interventions for canine atopic dermatitis reported good evidence for recommending the use of oral glucocorticoids and cyclosporine, fair evidence for topical triamcinolone spray, topical tacrolimus lotion, oral pentoxifylline or oral misoprostol and insufficient evidence for or against several other interventions including type-1 histamine receptor antagonists, tricyclic antidepressants and cyproheptadine (Olivry and Mueller, 2003). This review also concluded that there was fair evidence against recommending the use of other interventions. © 2014 Blackwell Verlag GmbH Zoonoses and Public Health 61 (suppl. 1) (2014) 3–9
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Systematic reviews can also highlight areas where there is insufficient evidence to assess the efficacy of interventions or where there are common methodological flaws in the available research, thereby providing direction and impetus for future basic and applied research in a specific area. For instance, a systematic review of surgical interventions for canine cranial cruciate ligament injury concluded that none of the surgical procedures evaluated in the review had sufficient data available in the literature to support them giving a consistent return of dogs to normal function (Aragon and Budsberg, 2005). In a systematic review of on-farm interventions to reduce faecal shedding of E. coli O157 in domestic ruminants, several of the interventions considered had only been evaluated using small scale field trials, in many cases using an artificial disease challenge (Sargeant et al., 2007). While the findings provide useful preliminary evidence that an intervention may work, they do not provide strong evidence that the intervention will work under real-life conditions. The same review noted that there were methodological flaws in several of the publications, including failure to report randomization to intervention groups in clinical trials. Thus, systematic reviews can identify knowledge gaps to target needed research and can also identify methodological issues that need to be considered when reading the existing literature and addressed when designing additional primary research studies. However, although the methods for developing systematic reviews of interventions in human health care are well developed, these methods may not be directly applicable to evaluate issues in animal agriculture and veterinary medicine (Sargeant et al., 2006a). An obvious difference between human health care and animal sciences is that animal studies encompass multiple species, and extrapolating results of studies from one species to another may not be appropriate. There are also important differences between human and veterinary medicine in the study designs used to address clinical questions. Randomized controlled trials (RCTs) provide the highest level of evidence for evaluating efficacy of interventions under real-world conditions (Higgins and Green, 2011) and are therefore preferred for inclusion in systematic reviews in both human and veterinary medicine. In human medicine, when a sufficient number of RCTs exist on a topic, systematic reviews of interventions often are restricted to include only results from RCTs. However, there are comparatively few RCTs published in veterinary medicine compared with human medicine, and therefore, observational studies are commonly used, particularly for interventions related to management practices. Additionally, challenge studies, where the investigator controls both the allocation to intervention and the disease occurrence (e.g. by deliberately challenging all study subjects with an infectious disease agent of interest and then randomly allocating study subjects to intervention groups), are often conducted in vet© 2014 Blackwell Verlag GmbH Zoonoses and Public Health 61 (suppl. 1) (2014) 3–9
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erinary research but are generally not used in human healthcare. Animal models of non-infectious diseases can be developed and used in the species of interest in veterinary medicine to evaluate potential interventions. In human medicine, studies using animal models can provide proof of concept for an intervention, but are not included in systematic reviews to evaluate real-world efficacy in humans. In human health care, patients are recruited for a study based on specified eligibility criteria and, with the exception of studies involving children or individuals with cognitive disabilities, provide informed consent for their own participation. In veterinary medicine, animal owners’/care-givers’ consent to participation on behalf of the animals that actually participate in the trial. This means that, in veterinary studies, there often are two ‘levels’ of selection and eligibility: that of the owner and that of the animal subjects. This may have implications for the comparability of trials evaluating the same intervention. There are additional factors to consider when conducting systematic reviews related to livestock species. Agricultural and husbandry practices vary substantively between countries, and livestock generally passes through distinct production stages during their lives which may involve very different dietary, housing and other management practices. Livestock populations are grouped and housed differently from human populations, meaning that aspects of trial design and analyses may differ between trials in livestock species and human trials. Research studies in livestock, particularly clinical trials, may be performed with individual animal intervention allocation and housing (often using an artificial disease challenge), small group intervention allocation and housing, or under typical commercial (field) conditions. When animals are housed in groups, the outcome may be determined based on group level variables, measurements on all animals within the group or subsampling of individuals within the group. Each of these methodological approaches will be associated with different statistical analyses. Therefore, when conducting systematic reviews of livestock-related questions, differences in study designs between studies addressing the same basic question will need to be considered when summarizing and interpreting results from multiple studies. Finally, human medical decisions are made based on the combination of scientific evidence about efficacy of the intervention, the balance of benefits and harms, and patient values and preferences. For livestock species, the balance of benefits and harms to the animal is important. However, there may be additional considerations, such as the costbenefit associated with the use of an intervention, food safety or animal welfare considerations, the producer or owner’s values and preferences, and for some issues the consumer’s values and preferences. Therefore, it is necessary to modify the existing protocols used for systematic 7
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reviews in the human healthcare field for use in systematically evaluating animal research. Despite these challenges, systematic reviews in animal agriculture and veterinary medicine will allow researchers to synthesize the current body of knowledge on targeted issues and lend increased credibility to findings in the field. Conclusion Systematic review is a structured method that has been widely used in human health care to summarize knowledge about the efficacy of interventions. The use of systematic reviews in animal agriculture and veterinary medicine is more recent, and there are difference between human and animal research that need to be considered. However, systematic reviews increasingly are being used in animal agriculture and veterinary medicine and offer an evidencebased method of summarizing primary research. Further articles in this series will overview study design issues when conducting systematic reviews, as well as providing details for each step of the systematic review process. Acknowledgements The authors thank Annette Wilkins for assistance with this manuscript. Funding and in-kind support was obtained from the Laboratory for Foodborne Zoonoses, Public Health Agency of Canada and the Canadian Institutes of Health Research (CIHR) Institute of Population and Public Health/Public Health Agency of Canada Applied Public Health Chair awarded to JM Sargeant. References Aragon, C. L., and S. C. Budsberg, 2005: Applications of evidence-based medicine: cranial cruciate ligament injury repair in the dog. Vet. Surg. 34, 93–98. Barnes, D. E., and L. A. Bero, 1998: Why review articles on the health effects of passive smoking reach different conclusions. JAMA 279, 1566–1570. Burns, M. J., and A. M. O’Connor, 2008: Assessment of methodological quality and sources of variation in the magnitude of vaccine efficacy: a systematic review of studies from 1960 to 2005 reporting immunization with Moraxella bovis vaccines in young cattle. Vaccine 26, 144–152. Chalmers, I., L. V. Hedges, and H. Cooper, 2002: A brief history of research synthesis. Eval. Health Prof. 25, 12–37. Cochrane, A. L., 1979: 1931–1971: A Critical Review, with Particular Reference to the Medical Profession. Medicines for the Year 2000, pp. 1–12. Office of Health Economics, London, UK. Cochrane Collaboration, 2013: The Cochrane Library. Available at: http://www.cochrane.org/tags/tags/cochrane-library (accessed on 14 April 2014).
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ing the CONSORT Statement. Zoonoses Public Health 57, 95– 104. Olivry, T., and R. S. Mueller, 2003: Evidence-based veterinary dermatology: a systematic review of the pharmacotherapy of canine atopic dermatitis. Vet. Dermatol. 14, 121–146. Pearson, K., 1904: Report on certain enteric fever inoculation statistics. BMJ 2, 1243–1246. Petticrew, M., 2001: Systematic reviews from astronomy to zoology: myths and misconceptions. BMJ 322, 98–101. Sackett, D. L., W. M. Rosenberg, J. A. Gray, R. B. Haynes, and W. S. Richardson, 1996: Evidence based medicine: what it is and what it isn’t. BMJ 312, 71–72. Sargeant, J. M., A. Rajic, S. Read, and A. Ohlsson, 2006a: The process of systematic review and its application in agri-food public-health. Prev. Vet. Med. 75, 141–151. Sargeant, J. M., M. E. Torrence, A. Rajic, A. M. O’Connor, and J. Williams, 2006b: Methodological quality assessment of review articles evaluating interventions to improve microbial food safety. Foodborne. Pathog. Dis. 3, 447–456. Sargeant, J. M., M. R. Amezcua, A. Rajic, and L. Waddell, 2007: Pre-harvest interventions to reduce the shedding of E. coli
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O157 in the faeces of weaned domestic ruminants: a systematic review. Zoonoses Public Health 54, 260–277. Sargeant, J. M., A. M. O’Connor, I. A. Gardner, J. S. Dickson, M. E. Torrence, and consensus meeting participants: I. R. Dohoo, S. L. Lefebvre, P. S. Morley, A. Ramirez, K. Snedeker, 2010: The REFLECT statement: reporting guidelines for randomized controlled trials in livestock and food safety: explanation and elaboration. Zoonoses Public Health 57, 105–136. Schulz, K. F., D. G. Alman, D. Moher, and for the CONSORT group, 2010: CONSORT 2010 Statement: Updated guidelines for reporting parallel group randomized trials. J. Clin. Epidemiol. 63, 834–840. Smith, M. L., and G. V. Glass, 1977: Meta-analysis of psychotherapy outcome studies. Am. Psychol. 32, 752–760. Snedeker, K. G., M. Campbell, and J. M. Sargeant, 2011: A systematic review of vaccinations to reduce the shedding of E. coli O157 in the feces of domestic ruminants. Zoonoses Public Health 59, 126–138.
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