introduction to systematic reviews in animal agriculture and veterinary medicine

REVIEW ARTICLE

Introduction to Systematic Reviews in Animal Agricultureand Veterinary MedicineJ. M. Sargeant1,2 and A. M. O’Connor3

1 Centre for Public Health and Zoonoses, University of Guelph, Guelph, ON, Canada2 Department of Population Medicine, Ontario Veterinary College, University of Guelph, Guelph, ON, Canada3 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 ani-

mal agriculture and veterinary medicine. In this article, we overview the method-

ology of systematic reviews and provide a discussion of their use. Systematic

reviews differ qualitatively from traditional reviews by explicitly defining a spe-

cific 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 crite-

ria), an assessment of the risk of bias for included studies and objectively summa-

rizing 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 agricul-

ture and veterinary medicine, the evidence-based medicine

movement encourages an evidence-based approach to deci-

sion-making, whereby the clinician precisely identifies a

clinical problem, searches for and critically appraises all rel-

evant 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

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 scien-

tific 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 rep-

licable method of identifying, evaluating and summarizing

© 2014 Blackwell Verlag GmbH � Zoonoses and Public Health, 2014, 61, (suppl. 1), 3–9 3

Zoonoses and Public Health

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-mak-

ers 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. origi-

nal research) for inclusion in the review, minimizing the

potential for selection bias. Selection of studies for inclu-

sion in a systematic review should be based on specific cri-

teria 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 ani-

mals and food safety (O’Connor et al., 2010; Sargeant

et al., 2010). When a sufficient number of studies with sim-

ilar 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

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 edu-

cation, 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 preven-

tive or therapeutic interventions (EFSA, 2010). The focus

of this article, and other articles in this series, will be on sys-

tematic reviews as they pertain to the evaluation of inter-

ventions. 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 pro-

grams 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 der-

matitis? (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 andTraditional Narrative Reviews

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, toFig. 1. Structured steps used to conduct systematic reviews of the liter-

ature (EFSA 2010).

© 2014 Blackwell Verlag GmbH � Zoonoses and Public Health 61 (suppl. 1) (2014) 3–94

Veterinary Systematic Reviews J. M. Sargeant and A. M. O’Connor

appraise the risk of bias in the included studies and to sum-

marize 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 differ-

ent, 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 Medi-

cal 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).

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 use-

able and reliable format (Hansen and Rieper, 2009). Criti-

cal 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 stu-

dent achievement (Glass and Smith, 1979). The concept of

‘systematic review’ is newer still and is defined to empha-

size 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 synthe-

sis 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 com-

mon early use of systematic research synthesis was in

human therapeutics. One important leader in this move-

ment 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 twen-

tieth 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

Good quality systematic reviews Traditional narrative reviews

Review topic –

what is the

question?

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

Finding data –

sources and

strategies

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

Not usually specified, often no attempt to find all relevant

literature. Therefore, potential for selection bias

Selection of

studies to include

Explicit description of the types of studies to be included;

other criteria specified to limit reviewer bias

Not usually specified. Therefore, potential for selection bias

Assessing risk of

bias in the

included studies

Formal assessment of the risk of bias in the original research

studies is examined in a systematic manner

Often do not evaluate risk of bias or differentiate between

methodologically sound studies and those with design flaws

or potential for biased results

Synthesizing study

results

Heterogeneity (difference in results) between studies is

explicitly described; results are statistically pooled where data

and methods are similar

Generally no formal statistical pooling of results; Often do not

consider differences in study methods or risk of bias in the

included studies

Inferences Conclusions are based on totality of evidence with a

consideration of the risk of bias

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 5

J. M. Sargeant and A. M. O’Connor Veterinary Systematic Reviews

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 rig-

orous manner with the experiences and expertise of stake-

holders (Sackett et al., 1996). This applied research appro-

ach 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 princi-

ples of managing healthcare knowledge in such a way that

it is quality assured, accessible and cumulative. As of Sep-

tember 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 recog-

nized as the gold standard for systematic reviews of the

effects of healthcare intervention studies. A handbook

describing the process of preparing and maintaining Coch-

rane 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, comple-

menting 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 health-

care 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 sup-

port 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 econo-

mists 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 andVeterinary Medicine

Systematic reviews are beginning to be used in veterinary

medicine and food safety for companion animals, food ani-

mals 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, com-

pare the efficacy between interventions or can provide data

as input into risk assessment models. For instance, a sys-

tematic review of multiple pharmacological interventions

for canine atopic dermatitis reported good evidence for rec-

ommending the use of oral glucocorticoids and cyclospor-

ine, fair evidence for topical triamcinolone spray, topical

tacrolimus lotion, oral pentoxifylline or oral misoprostol

and insufficient evidence for or against several other inter-

ventions 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.



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 suffi-

cient 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 inter-

ventions 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 pro-

vide 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, includ-

ing 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 themethods for developing systematic

reviews of interventions in human health care are well devel-

oped, these methods may not be directly applicable to evalu-

ate 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) pro-

vide 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 sys-

tematic reviews in both human and veterinary medicine. In

humanmedicine, 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 medi-

cine compared with human medicine, and therefore, obser-

vational studies are commonly used, particularly for

interventions related tomanagement 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-

erinary research but are generally not used in human health-

care. 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 system-

atic 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 partici-

pation. 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 veteri-

nary studies, there often are two ‘levels’ of selection and eli-

gibility: 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 conduct-

ing systematic reviews related to livestock species. Agricul-

tural 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 live-

stock, 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 com-

mercial (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 con-

ducting systematic reviews of livestock-related questions,

differences in study designs between studies addressing the

same basic question will need to be considered when sum-

marizing 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 cost-

benefit 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 neces-

sary to modify the existing protocols used for systematic



reviews in the human healthcare field for use in systemati-

cally 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, sys-

tematic reviews increasingly are being used in animal agri-

culture and veterinary medicine and offer an evidence-

based 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 evi-

dence-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 method-

ological 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 Partic-

ular 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).

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 assess-

ments 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 medi-

cine 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 crit-

ical appraisal of review articles on the effectiveness of con-

servative 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 educa-

tion. 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 sci-

ence. 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 Random-

ized Controlled Trials for livestock and food safety by modify-



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 zool-

ogy: 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

O157 in the faeces of weaned domestic ruminants: a system-

atic 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 guide-

lines 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 psycho-

therapy 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.



introduction to systematic reviews in animal agriculture and veterinary medicine

Documents