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B I O L O G I CA L C O N S E RVAT I O N 1 3 2 ( 2 0 0 6 ) 4 0 9 –4 2 3

available at www.sciencedirect.com

journal homepage: www.elsevier.com/locate/biocon

Are review articles a reliable source of evidence to


support conservation and environmental management?
A comparison with medicine

Philip D. Roberts*, Gavin B. Stewart, Andrew S. Pullin


Centre for Evidence-Based Conservation, School of Biosciences, University of Birmingham, Edgbaston, Birmingham, West Midlands B15
2TT, UK

A R T I C L E I N F O A B S T R A C T

Article history: Review articles are important sources of information and often the only source of evidence
Received 19 December 2005 used by decision makers in conservation and environmental management to assess effec-
Received in revised form tiveness and impact of interventions and other actions. Recent developments in the field of
21 April 2006 medicine and public health have established ‘systematic review’ guidelines to minimise
Accepted 27 April 2006 bias and explicitly document methodology, allowing replication and updating in light of
Available online 13 June 2006 further advances. The aim of this article was to assess the methodological and reporting
rigour of reviews from the disciplines of conservation, ecology and environmental manage-
Keywords: ment (referred to as ‘‘ecological reviews’’). This was achieved by comparing them to med-
Systematic review ical systematic reviews, using 27 detailed criteria well established in medicine. When
Evidence-based practice compared with medical systematic reviews, ecological reviews were more likely to be prone
Review methodology to bias, lacking details in the methods used to search for studies, and were less likely to
Decision-making assess the relevance of studies, quality of the original experiments and to quantitatively
Meta-analysis synthesise the evidence. Overall, ecological reviews show lower quality and greater varia-
tion in reporting style and review methods. To address this, reviewers could use a system-
atic review approach and journals could provide more explicit guidelines for the
preparation and production of review articles.
 2006 Elsevier Ltd. All rights reserved.

1. Introduction sometimes very complex or controversial subjects and can


provide connections between past and future research direc-
The literature review is an established feature of many scien- tions (Gates, 2002). They can act as efficient tools to assist in
tific journals, across a wide diversity of disciplines. Reviews knowledge transfer, raising awareness of research findings
allow comparisons to be drawn between different sets of and encouraging the possible adoption of management alter-
studies, often enabling synthesis of independent data sets, natives (CRD, 2001).
and are therefore a necessary part of the scientific process Studies often have conflicting findings and reviews are
(Arnquist and Wooster, 1995). As new facts are presented, necessary to investigate the biological or methodological rea-
their relation to old ones should be pointed out (Chalmers sons for this variation. For example in medicine, assumptions
et al., 2002; Egger et al., 2003). For the majority of scientists of the benefits of routine antiarrhythmic therapy based upon
and practitioners a good review can be a valuable commodity. human biological plausibility led to its widespread use to pre-
They are often the first port of call for useful summaries of vent acute myocardial infarction. However, subsequent

* Corresponding author: Tel.: +44 121 4144090; fax: +44 121 4145925.
E-mail address: pdr387@bham.ac.uk (P.D. Roberts).
0006-3207/$ - see front matter  2006 Elsevier Ltd. All rights reserved.
doi:10.1016/j.biocon.2006.04.034
410 B I O L O G I C A L C O N S E RVAT I O N 1 3 2 ( 2 0 0 6 ) 4 0 9 –4 2 3

empirical studies demonstrated that antiarrhythmic therapy Pullin and Knight, 2001; Sutherland et al., 2004). Currently, it
actually increased patient mortality (CAST, 1989; Woolf, is unclear how rigorous existing narrative reviews are and
2000). Due to the mounting number of cases similar to that to what extent systematic review methodologies are already
above, Cochrane (1979) issued a challenge to organise critical being utilised. For example, do authors carry out an explicit
summaries of the best available evidence for each specialty and detailed search of all literature sources, or do they simply
that would be readily available and regularly updated. This grab a number of papers from their file-drawer (Mulrow, 1987;
challenge was gradually accepted by both practitioners and Rosenthal, 1979)? In addition to the standard electronic
policy makers, causing a ‘‘scientific revolution’’ within the sources of published scientific literature (e.g. Web of Science,
fields of medicine and public health, shifting both from a sub- Science Direct, Scopus), authors can carry out extensive grey
jective experience-based approach to a rigorous evidence- literature searches of non-governmental and governmental
based approach to practice (Sackett and Rosenberg, 1995). organisations’ web based resources, contact external subject
Within this evidence-based approach new frameworks for experts for the identification of any non-published or internal
the reviewing of scientific data (evidence) have developed, reports they may have contributed to and/or make arrange-
(see the UK’s National Health Service Centre for Research ments to search an organisation’s library. These additional
and Dissemination (NHS CRD) report 4, 2001 and The Coch- searches, although time consuming, are an integral part of
rane Collaboration Handbook – Higgins and Green, 2005) the systematic review process and can often lead to the iden-
and new independent organisations such as the Cochrane tification of important unpublished datasets, theses and tech-
Collaboration have been established. The Cochrane Collabo- nical reports, which are generally overlooked as they are not
ration provides readily available, up-to-date, accurate infor- indexed in the standard electronic databases.
mation about the effectiveness of different healthcare Over the past decade there have been a number of reviews
interventions. This is achieved through the production and within the conservation and environmental management dis-
dissemination of ‘‘systematic reviews’’, an explicit methodol- ciplines which have incorporated quantitative meta-analyti-
ogy for the detailed exploration, critical evaluation and inter- cal techniques to synthesise evidence (e.g. Levine et al.,
pretation of all available evidence that is relevant to a 2004). However, these reviews are still open to the same
particular subject (CRD, 2001). Systematic reviews are scien- biases as narrative reviews if the evidence being synthesised
tific investigations in themselves; they have pre-planned has been chosen subjectively, without an adequate search
methodologies (protocols) and an assembly of original studies strategy and inclusion/exclusion criteria to identify all rele-
as their ‘‘subjects/population’’. They are of particular value in vant studies (CRD, 2001).
combining a number of separately conducted primary stud- In this paper we: (1) assess the methodological rigour of
ies/investigations, sometimes with very conflicting findings, current conservation, ecology and environmental manage-
and when possible synthesise their results quantitatively ment reviews, hereafter referred to as ‘‘ecological reviews’’,
using strategies that limit bias and random error (Egger using the criteria recently adopted by medicine (see CRD,
et al., 2003; Mulrow, 1994). 2001; Higgins and Green, 2005); (2) quantitatively compare
Within the disciplines of conservation and environmental these results against an assessment of recently published
management the standard approach to reviewing literature is medical ‘‘gold standard’’ Cochrane systematic reviews, to
still the traditional ‘‘narrative review’’ (Gates, 2002). Narrative establish if there are any deficiencies in the methodology
reviews normally provide only a qualitative assessment of the and reporting styles of the current ecological reviews; and
published results and are primarily based on the experience (3) conclude by outlining the ‘systematic review’ approach
and subjective judgement of the author(s). This can lead to for adoption within ecological and environmental disciplines.
biases towards a particular side of an issue, instead of being
based on the best evidence we have available to us. They also 2. Methods
frequently lack methodological transparency and therefore
cannot easily be repeated or updated on a regular basis (Egger 2.1. Search strategy and inclusion criteria
et al., 2003; Mulrow, 1994). Review articles have been identi-
fied as a leading source of information used by nature conser- To identify reviews applicable to this study, the ecological
vation practitioners when producing management plans (this journals section of the ISI Journal Citation Reports of Web of
includes site, species and habitat action plans) (Pullin et al., Knowledge (http://wok.mimas.ac.uk/) was searched using
2004). However, the need for a more systematic use of evi- the impact factor sorting facility to identify the leading 40
dence in the production of conservation management plans ecological journals, accepting only those which stated within
is still required. There are numerous examples of conserva- their ‘aims and scope’ or ‘advice to authors’ that they pub-
tion advice and actions being undertaken without a traceable lished ‘reviews’ (an article that provides a narrative synthesis
source of evidence to show why the practitioner came to their of a topic’s literature) or ‘syntheses’ (similar to a review arti-
decision (Sutherland and Hill, 1995). In the absence of evi- cle, provides new quantitative syntheses, meta-analysis or
dence, managers rely on personal experiences or revert to modelling of the data where applicable, and discusses new
‘‘traditional’’ methods, especially in the cases such as grazing directions for future research). Starting from the issue cur-
regimes and coppicing (Pullin and Knight, 2001). rently available online, we searched the last 12 issues of each
There has been a series of calls for the use of the rigour journal on 12th October 2005. To allow direct comparison with
inherent in systematic review methodology in conservation the medical and public health disciplines that already utilise
and environmental management disciplines to provide deci- systematic review methodology, only those review articles
sion-makers with the best available evidence (Pullin, 2003; or synthesis papers which had an applied conservation,
B I O L O G I C A L C O N S E RVAT I O N 1 3 2 ( 2 0 0 6 ) 4 0 9 –4 2 3 411

ecological or environmental management element, i.e. were mented and repeatable methods for how data was extracted
investigating the ‘‘effectiveness’’, ‘‘impact’’ or ‘‘effect’’ of an from each of the studies accepted within the review synthe-
intervention, management policy or natural process, were sis; (13) provide a formal assessment and estimation of the
considered for inclusion within the assessment of methodol- possible risk of publication bias of those studies accepted
ogies. In total, the selection criteria yielded 73 (26%) of 279 re- within the final synthesis of the review, (e.g. using funnel
view or synthesis articles identified within the leading 40 plots, or similar assessment, such as Egger tests to assess
ecological journals. the distribution of effect sizes according to sample size or in-
Medical reviews were identified by searching the online verse variance (CRD, 2001)); (14) provide a qualitative synthe-
version of the Cochrane Collaboration Library for the most re- sis of the evidence in the text of the review and/or tabulated
cent review articles (searched on 17th October 2005). Using a each accepted studies’ findings; (15) plan to undertake a
random number generator, 73 reviews were selected. The quantitative synthesis of the evidence according to the meth-
Cochrane Collaboration style systematic review was chosen ods section of the review; (16) undertake a quantitative anal-
as the ‘gold standard’ of medical review articles (Jadad ysis of the evidence when possible; (17) performed a meta-
et al., 1998). The Cochrane Collaboration provides detailed analysis (a statistical technique that combines the findings
methodological guidelines (see Higgins and Green, 2005) that of two or more studies for the purpose of drawing general
authors are advised to follow giving Cochrane reviews a stan- conclusions, developing support for hypotheses, and/or pro-
dardised format. The guidelines are intended to help authors ducing an estimate of overall management effect); (18) inves-
to be systematic and explicit in the way they approach ques- tigate any sources of heterogeneity within the dataset; (19)
tions they pose and how they can derive answers to those perform sensitivity analysis upon the data; (20) investigate
questions. They provide guidance on: formulating a question; whether there was appropriate power within analyses, nor-
locating and selecting studies; quality assessment of studies; mally through post hoc power analysis; (21) report the key find-
collecting, analysing and presenting results; and how to inter- ings of the review; (22) reference all studies used within the
pret, draw conclusions and provide recommendations from review; (23) provide an appendix/list of those reviews ex-
the output of the analyses. Each review also undergoes peer cluded from the review but viewed at full text (this allows
review prior to being published online on the Collaboration’s readers to assess these studies for themselves if so desired
library website (http://www.cochrane.org/) and the authors and provides a wider reference source, possibly identifying
can publish their reviews in their appropriate subject unknown grey literature, which might be suitable for readers
journals. studying a closely related subject); (24) identify an evidence
gap/lack of data to properly answer the main question of
2.2. Assessment criteria and data extraction the review; (25) identify other evidence-gaps or areas lacking
knowledge in light of the review’s findings; (26) provide rec-
Both sets of captured reviews were assessed against the fol- ommendations for future topics/questions that still require
lowing explicit criteria of 27 methodological and reporting as- investigation; and (27) advise on the methodology of future
pects, adapted from published guidelines for the synthesis of experiments (incl. appropriate sample sizes and experimental
information (CRD, 2001; Higgins and Green, 2005; Mulrow, designs).
1987; Rosenthal, 1991): Did the authors: (1) produce an explicit
a priori protocol, which could be available online (a standard 2.3. Quantitative analysis
practice for Cochrane reviews and/or outlined within the re-
view article); (2) explain the background of the review; (3) The methodological and reporting characteristics were re-
clearly state a question that the review was to address; (4) corded as being either present or absent for each of the 146 re-
clearly define the question elements (e.g. PICO – Population, views (73 ecological and 73 Cochrane, see Appendix A for
Intervention (or Management/Process of interest), Compara- reference list of reviews). These characteristics were used to
tors, Outcomes of interest); (5) define search terms used to classify the reviews into hierarchical groups using two way
identify sources of evidence (this could be provided within re- indicator species analysis (TWINSPAN) (Hill, 1979). The analy-
view, as supplementary material or at organisation’s website); sis was limited to three sequential divisions that could poten-
(6) document a detailed systematic literature search of tially produce eight groupings, which show the level of
sources (e.g. use of specific databases and/or reference list); variation within the quality of the reviews. Complimentary
(7) search for unpublished ‘grey’ literature which is held by ordination using detrended correspondence analysis (DCA)
non-governmental organisations, governmental departments (Hill, 1974) was conducted, based upon the same methodolog-
and/or charities; (8) define inclusion/exclusion criteria for ical and reporting characteristics to investigate the relation-
identification of relevant evidence; (9) document reasons for ship between the ecological and Cochrane reviews. The
inclusion/exclusion for each study (again, this is standard TWINSPAN groupings were superimposed on the ordination
procedure for medical systematic reviews and provided with- plot to allow each ecological and Cochrane review to be easily
in appendices of online supplementary material); (10) use two identifiable. The median Eigenvalue scores for the ecological
or more reviewers to undertake inclusion/exclusion and data and Cochrane reviews were calculated and compared using
extraction to limit selection bias; (11) undertake an assess- Mann–Whitney U tests (Siegel, 1956) to investigate if either
ment of each studies quality/validity (e.g. did the review as- groups’ methodological and reporting qualities significantly
sess one or more of the following features – experimental differed from one another.
designs, sampling accuracy, timescales, baseline surveys, To test whether ecological and Cochrane reviews differed
scales, pseudo-replication); (12) provide standardised, docu- significantly in each of the 27 methodological and reporting
412 B I O L O G I C A L C O N S E RVAT I O N 1 3 2 ( 2 0 0 6 ) 4 0 9 –4 2 3

Table 1 – Results of the comparative assessment of ecological and Cochrane review articles against 27 methodology and
reporting characteristics, with the number of reviews fulfilling each characteristic and the results of v2 tests or Fishers
exact test presented
Characteristics of methodology Ecological Cochrane Probability

Planning and search (n = 73) (n = 73)


Production of an explicit repeatable documented a priori protocol 0 73 <0.0001
Explained background to the review 73 73
Defined question 65 73 0.0032
Question elements: population, intervention, comparator and outcome defined 14 70 <0.0001
Defined search terms to be used to identify sources of evidence 14 66 <0.0001
Documented detailed systematic literature search of all sources (incl. databases, ref lists, proceeds) 22 73 <0.0001
Searches for unpublished ‘grey’ literature 21 47 <0.0001

Identification of the evidence and potential biases


Defined inclusion/exclusion criteria for identification of relevant (evidence) studies 25 73 <0.0001
Reasons for inclusion/exclusion documented for each study 1 70 <0.0001
Inclusion/exclusion controlled (KAPPA) 0 70 <0.0001
Assessment of the each studies quality/validity
1. Experimental designs 23 69 <0.0001
2. Sampling accuracy
3. Appropriate timescales
4. Baseline survey
5. Scale
6. Pseudo-replication
Data extraction methodology documented and repeatable 15 51 <0.0001
Estimation of publication bias 6 17 0.0125

Data-synthesis and analysis


Descriptive qualitative synthesis 73 73
Planned quantitative synthesis of evidence 29 73 <0.0001
Undertook quantitative synthesis 27 59 <0.0001
Performed meta-analysis 8 49 <0.0001
Investigation of sources of heterogeneity
1. Sub-group 12 36 <0.0001
2. Meta-regression
Sensitivity analysis (excel of certain data, etc.) 0 23 <0.0001
Investigation to whether there was appropriate power to accept/reject H0 or H1 2 3 0.5000

Reporting
Reporting the key results of the review 73 73
Provides references of all studies within the review 73 73
Identification of evidence gap for the main question 49 46 0.6025
Identified other evidence gaps related to subgroup/sensitivity analyses 48 51 0.5951
Recommendations for future studies 64 70 0.0706
Advised on future experimental designs and/or sample sizes for future experiments 34 41 0.2464
Listed excluded studies in reference list or appendix/online material 0 70 <0.0001

For further details of the assessment procedures see Section 2.

characteristics, frequency counts for each characteristic of comes) of the question under review. Cochrane reviews de-
both review groups were collated and compared using two- fined a detailed search strategy: including giving the search
way classification chi-squared tests (26 of 27 variables) or terms used, sources searched (including computer databases,
Fisher’s exact test (when expected frequencies were less than conference proceedings and reference lists) and included
five, as for characteristic 3 (Table 1)). For all analyses values of unpublished ‘grey’ literature. Ecological reviews were limited
P < 0.05 were regarded as statistically significant. The analy- in their recording of the search methods utilised for the cap-
ses were carried out using a combination of Excel (XP), Stats- ture of evidence, with only 30% (22/73) of authors reporting
Direct (version 2.5) and PC-ORD (version 4.0). any details of the sources they used to acquire evidence and
less than 20% (14/73) reporting the search terms used.
3. Results When identifying the relevant evidence and potential
biases from the original studies, all Cochrane reviews defined
Cochrane reviews were more rigorous when planning and the inclusion/exclusion criteria for the identification of rele-
searching for sources of evidence (Table 1). They followed vant studies and documented the reasons for inclusion/
an explicit protocol of documented methods, which were exclusion of all studies viewed at full text, controlling the pro-
planned a priori to reduce bias, defined the question clearly, cedure by having two or more authors undertake study selec-
and stated the components (subjects, intervention and out- tion. However, only 34% (25/73) of ecological reviews provided
B I O L O G I C A L C O N S E RVAT I O N 1 3 2 ( 2 0 0 6 ) 4 0 9 –4 2 3 413

inclusion criteria and in only 1 of 73 reviews were details of thesis of the evidence. Cochrane reviewers undertook quanti-
excluded studies provided. Over 90% (69/73) of Cochrane re- tative synthesis of the evidence (involving meta-analysis) and
views assessed the quality of the original studies and 70% investigated potential sources of heterogeneity using sub-
provided clear methodology of how evidence was to be ex- group analysis or meta-regression, while ecological reviewers
tracted from the original studies, compared to just 32% (23/ either neglected to mention heterogeneity (75%, 55/73) or
73) of ecological reviews assessing quality and only 21% (15/ used qualitative methods to explain potential sources, but
73) explaining data extraction methods. did not actually investigate these (8%, 6/73). In only 16% (12/
All ecological and Cochrane reviews provided a descriptive 73) of ecological reviews were formal quantitative methods
qualitative synthesis of the evidence; furthermore, all authors used to explain any heterogeneity within the dataset and
of Cochrane reviews documented that they planned to under- the sources of heterogeneity were never demonstrably identi-
take quantitative synthesis, providing the methodology to ex- fied a priori. Finally, when reporting the findings of the review
tract and analyse the data, but only 40% (29/73) of ecological there were no significant differences between the two types
review authors stated that they planned a quantitative syn- (Table 1), with the exception that Cochrane reviews provided

77

34 14

20

122

12
125
9

38
58
100 127

1, 25, 30, 39, 52, 53 3 55 32


89 5
101 116
15, 46, 56,138 64
133 102
11 123 126
51, 65, 71 10
18 4 144 132 13 169 131
22 115 68 19 6 54 145 2, 103 23, 44
70 105 90, 104
80
40, 139 74 91 110 119 98 35 113 106 8 108
92 21 37 36, 75
47, 121 136 83 16 62 78, 109, 146 85 17, 93, 129
49, 118 67, 137 59 124
111 114 81, 140 73 76 142 88 26, 84
29 130 33 135
43 112 61, 143, 28, 94 50 41
31 7 134 66
63 57
99 96
60 97 82 117
128 27 ..87 42, 45
24 72 141
107 120 95

86
48
79

Fig. 1 – DCA ordination with TWINSPAN groups overlaid. Ecological reviews (open symbols) and Cochrane reviews (closed
symbols). The numbered labels refer to the individual reviews as listed in Appendix A. (d) Cochrane reviews including meta-
analysis. (j) Cochrane reviews without meta-analysis, (s) Ecological reviews containing meta-analysis, (·) Ecological reviews
which undertook quantitative synthesis, investigated heterogeneity and assessed the quality of the original studies, (h)
ecological reviews which undertook quantitative synthesis (not meta-analysis) and investigated heterogeneity, (e) ecological
reviews which clearly defined question and included some search details and included meta-analysis, (,) ecological reviews
which defined inclusion/exclusion but qualitatively synthesised evidence (n) ecological reviews which solely qualitatively
synthesised an unknown amount of the available evidence. Axis 1 eigen = 0.18 and axis 2 eigen = 0.06.
414 B I O L O G I C A L C O N S E RVAT I O N 1 3 2 ( 2 0 0 6 ) 4 0 9 –4 2 3

a reference list of those articles which were viewed at full text odology to be used (Higgins and Green, 2005). All 73 Coch-
but rejected from the final review, while this was absent from rane reviews assessed in this study produced protocols and
all ecological reviews. disseminated them to stakeholders (individuals, groups or
The differences in methodological and reporting charac- organisations that are affected by and/or have an interest
teristics were confirmed by classification (TWINSPAN) and in a particular issue) to receive comments/amendments
ordination (DCA). There is a distinct clustering of the Coch- prior to undertaking the full review. All report the literature
rane reviews separate from the ecological reviews, which sources (e.g. databases, journals to be hand searched) and
were more dispersed across both axes of the ordination 90% (66/73) list the search terms used for each source, as
(Fig. 1). The separation of the two review groups was highly well as including this information in the methods section
significant on both axes (Axis 1: ecological reviews median of the review. This gives the reader confidence that the
Eigen score = 59, Cochrane reviews mean Eigen score = 150, authors have identified all available sources relevant to the
U = 232, P < 0.0001; and Axis 2: ecological review median Eigen subject being reviewed and therefore confidence in the find-
score = 68, Cochrane review mean Eigen score = 39, U = 4875.5; ings of the review. In stark contrast, none of the ecological
P < 0.0001). Overall, reviews that undertook or planned quan- reviews reported that they had undertaken the protocol pro-
titative synthesis of the captured data had higher first axis cess, with only 30% (22/73) reporting the literature sources
scores, as shown by the Cochrane reviews and ecological searched and less than 20% (14/73) listing the search terms
meta-analyses (TWINSPAN group’s d, j and s, see Fig. 1). used. This shortage in reported detail results in the reader
Axis 2 relates to the searching and reporting characteristics being unsure if a comprehensive synthesis of the evidence
of the reviews. Those reviews which lacked enough detail to was undertaken and to what extent the conclusions drawn
be easily repeated (e.g. lacking detail of how the evidence by the authors, can be relied upon.
was identified and how it was extracted from the original pa- The aim of the study inclusion/exclusion phase of the
per) all had low second axis scores (TWINSPAN group’s n and Cochrane reviews is to identify those studies that help to an-
e, see Fig. 1), whilst those which could be repeated and there- swer the question(s) being addressed by the review. In 100% of
fore easily updated in light of new research had high second Cochrane reviews, detailed inclusion/exclusion criteria were
axis scores (TWINSPAN groups d, j, s, and h, see Fig. 1). documented, giving further transparency and repeatability
of the review methodology. In contrast, only 34% (25/73) of
4. Discussion the ecological reviews gave details of the inclusion/exclusion
criteria that they were using for the identification or applica-
Our results show that systematic methods of searching, ble studies. The study inclusion/exclusion phase of the sys-
selecting and assessing the relevance and quality of data tematic review follows logically from the defined review
along with quantitatively synthesising evidence (all consis- question, as components of the question (the population,
tent with the Cochrane review methodology) are not routinely intervention, comparator and outcome) are used to create cri-
nor rigorously used in applied ecological subjects such as con- teria against which each of the identified studies from the
servation and environmental management. On a positive searches are assessed.
note, the meta-analytical element is now becoming more Reviews that undertake quantitative, meta-analytical
commonplace. All the assessed ecological reviews provided techniques provide increased statistical power when com-
an overview of the topic; however, they would benefit from pared to individual studies, allowing for the assessment of
using systematic review guidelines, as followed by Cochrane small effects and conditions of relatively low event rates
reviews, to increase the repeatability of their methodology, and, compared to traditional narrative reviews, allow for a
allowing readers to evaluate whether all available evidence quantitative and objective analysis of the evidence (Arnquist
had been captured. and Wooster, 1995; Egger et al., 2003). The consistency of rela-
Both narrative and systematic reviews are retrospective, tionships between included studies can be investigated,
observational pieces of research, fully dependant on the ex- allowing the assessment of their direction and magnitude;
tent to which review methods have been used to minimise data inconsistencies and conflicts can be investigated and ex-
both bias and random error. This important feature is key plained (CRD, 2001). In addition, the diversity of multiple
to distinguishing the traditional review from a systematic re- studies analysed within a systematic review provides an
view (Egger et al., 2003; Higgins and Green, 2005). Within the interpretive context that can be reliably generalised across
last decade the traditional medical narrative review has been differing situations/sites, which would otherwise not have
identified as being of poor quality and rife with personal been available from either a traditional review or a single
biases from the reviewers’ own opinions, and as such repre- large study (Egger et al., 2003; Hedges and Olkin, 1985). How-
sents an unreliable source of information (CRD, 2001; Glas- ever, although there are distinct advantages of the use of
ziou et al., 2001; Mulrow, 1994). Without the guidance of meta-analytical techniques, the results derived are only as
formal rules, review author(s) inevitably disagree about is- good as the data being synthesised. If the review lacks a com-
sues such as what types of studies are appropriate to in- prehensive search strategy, it is likely to suffer from a degree
clude, and how to extract or summarise the evidence from of publication bias, when the publication of research depends
each of the individual studies. Cochrane reviewers follow on the nature and direction of the study results, where stud-
formal rules to minimise biases by documenting a detailed ies in which an intervention is not found to be effective are
a priori protocol of the search strategy, the selection criteria generally not published. Due to this, reviews which fail to in-
to identify appropriate studies, assessment of their quality clude unpublished studies (‘grey literature’) may overestimate
(validity) and details of the extraction and synthesis meth- the true effect of an intervention resulting in false positive
B I O L O G I C A L C O N S E RVAT I O N 1 3 2 ( 2 0 0 6 ) 4 0 9 –4 2 3 415

conclusions being drawn, which if acted upon could be more between the various studies. By using standardised appraisal
resource intensive for the organisation than if they had ini- forms, the uniformity of the assessment is achieved (for
tially commissioned a comprehensive, systematic review of examples of appraisal forms that can be adapted for use with
all the evidence (Glasziou et al., 2001; Higgins and Green, ecological studies see http://www.sign.ac.uk/methodology/
2005; Scargle, 2000). Overall, those ecological reviews which checklists.html) and, by having two or more reviewers per-
used meta-analytical techniques also contained more of the forming the appraisal, biases can be minimised and repeat-
27 methodology and reporting characteristics; however, they ability demonstrated. The information gained from a good
still lacked consistency when reporting details of the search quality assessment can be used to determine the strength
criteria used to identify their sources of evidence and in gen- of inferences derived within the review (Glasziou et al., 2001).
eral failed to investigate both publication bias and any Fifth, the synthesis of evidence should be undertaken in a
sources of heterogeneity within the dataset. This is clearly repeatable systematic manner. This can be achieved through
shown in the TWINSPAN classification and DCA ordination a qualitative synthesis complemented by the use of formal
as the majority of the quantitative reviews were grouped to- statistical techniques for pooling and analysing data from
gether with higher axis 1 and 2 scores than those reviews that numerous sources (e.g. meta-analysis) when appropriate
qualitatively summarised the available evidence. The close (Arnquist and Wooster, 1995; Gates, 2002).
grouping of the Cochrane reviews (TWINSPAN group’s d and Sixth, faced with limited time to read the whole review,
j) illustrates that all 73 reviews were prepared following the many readers will go directly to the conclusion section.
same guidelines. The biggest difference among Cochrane re- Therefore this section should be clearly worded, based only
views is method of synthesis, with some reviews capturing on the evidence reviewed, and should discuss the strength
data clearly inappropriate for quantitative treatment. How- of the evidence and applicability of the results.
ever, review quality was variable with minor omissions of Finally, we advocate that all scientific journals that publish
information (e.g. future experimental design details, investi- reviews should revise their guidelines to encourage the use of
gating heterogeneity of the data) by those reviews which ob- systematic review methodology. The advantages of the sys-
tained a lower axis 2 score. tematic review process have already been demonstrated in
medicine and public health, allowing improvements in the
5. Recommendations impact, quality and power of review articles (Glasziou et al.,
2001). Ecology is slow in its acceptance of this approach with
In our view, improving the impact and quality of ecological re- the first two systematic reviews having only recently been
views will be highly beneficial in the applied fields of conser- published (Stewart et al., 2005; Tyler et al., 2006). In addition,
vation and environmental management, but requires both we also propose that in future, agencies that commission re-
authors and publishers to follow several key stages of the sys- views demand, when appropriate, the rigour provided by this
tematic review process (Pullin and Stewart, in press). First, the methodology. The use of this approach would allow for de-
author(s) should define a question similar to formulating a tailed assessments of the effectiveness of conservation and
hypothesis for primary research. This allows the reader to environmental management techniques undertaken by agen-
understand the scope of the review’s question and its aims cies and provide important evidence on environmental
from the outset (Dennison and Kirk, 1990; Light and Pilemar, impacts.
1984), and guides the subsequent stages of study inclusion
and data synthesis. Acknowledgements
Second, as the aim of the systematic review process is to
answer a question based on the best available evidence, The authors thank NERC (NE/C508734/1) and English Nature for
including both published and unpublished ‘grey literature’, a grant support for this project, our colleagues at the CEBC, Prof.
comprehensive and documented search strategy is required. Khalid Khan for his advice, the four anonymous reviewers and
This search strategy should be documented in the final article Tamara Kabat who proofed the manuscript and provided valu-
to allow the review to be repeated/updated at regular inter- able statistical and editing recommendations.
vals (e.g. every five years) or in the light of new advances.
Third, the use of explicit inclusion/exclusion criteria for Appendix 1
identifying all relevant evidence to the question should be
stated (e.g. based on certain methodological criteria of the ori-
ginal studies or/and on population characteristics by includ- The references of the reviews assessed in the article, in numer-
ing wild and excluding captive based studies). By ical order as presented in the DCA ordination plot (Fig. 1).
documenting this process, preferably a priori, pre-formed
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