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3 Cardiovascular Nutrition Laboratory, Jean Mayer USDA Human Nutrition Research Center on Aging, Tufts University, Boston, MA 02111; 4 Office of Dietary Supplements, NIH, Bethesda, MD 20892; 5 Tufts Evidence-Based Practice Center, Institute for Clinical Research and Health Policy Studies, Tufts Medical Center, Boston, MA 02111
* To whom correspondence should be addressed. E-mail: alice.lichtenstein{at}tufts.edu.
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ABSTRACT |
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Introduction |
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TOPABSTRACTIntroductionLITERATURE CITED |
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There is a long history for the use of systematic reviews in the medical community to develop clinical and public health practice guidelines (2,3), set research agendas (1), and formulate scientific consensus statements (4,5). The use of systematic reviews to address nutrition-related issues is more recent (6–10). Nevertheless, there is a wide range of nutrition applications for which a systematic review process has been used or is being considered (Table 1). Although many of these applications are similar to those used in the areas of medicine and public health, characteristics unique to nutrition-related topics (e.g. essentiality, habitual exposure) necessitate the development of a more complex set of research questions and approaches to the decision-making process than have traditionally been encountered in other fields (11). It should be noted that as systematic reviews are increasingly being performed and published for nutrition-related topics, the term "systematic review" has been subjected to various modifications to include evidence-based review, systematic evidence-based review, and evidence-based systematic review. In this article, we use the term systematic review, which is the common usage in medicine and other disciplines.
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Examples of recent systematic reviews of nutrition-related topics
Three examples of systematic review applications are summarized for nutrition-related topics: effectiveness and safety of vitamin D in relation to bone health (10), effects of soy on health outcomes (12), and health effects of (n-3) fatty acids on arrhythmogenic mechanisms in animal and isolated organ/cell culture studies (Table 2) (13). These examples were selected because they illustrate the comprehensive and flexible nature of the systematic review process. Although similar steps were followed, they were conducted by 2 evidence-based practice centers (Tufts Medical Center Evidence-Based Practice Center and University of Ottawa Evidence-Based Practice Center). The inherent flexibility of the systematic review methodology is illustrated by the topics that address issues related to a single nutrient, vitamin D and bone health, complex nutritional interventions, soy protein/isoflavones and health outcomes, and multiple experimental models and outcomes, (n-3) fatty acids, and animal/isolated organ/cell culture. They also include study design foci that address issues related to animal/in vitro, (n-3) fatty acids combination of observational and intervention human studies, soy and health outcomes, exclusive reliance on randomized clinical trials, and several questions for vitamin D and bone health.
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Thousands of systematic reviews on healthcare topics have now been published and standards for reporting of systematic reviews have been proposed (14–17). Several organizations such as the Cochrane Collaboration (18) and the Agency for Healthcare Research and Quality (19) have established guidance for conducting systematic reviews. Here, we describe the common principles of conducting a systematic review. A systematic review should include a detailed description of the approach and parameters used to ensure completeness in identifying the available data, rationale for study selection, method of critical appraisal of the evidence, and method of analysis and interpretation. As will become apparent, depending on the question of interest or on the basis of new data, there are opportunities to revisit and refine decisions made at certain points. Critical to the integrity of the process is thorough documentation at all steps. The approach presented assumes that persons well versed in systematic review methodologies will be part of the research team and the product will be used by other groups as one component of a decision-making process.
Identify staffing. The actual work and associated decisions of conducting the systematic review are the responsibility of a multidisciplinary research team. However, at appropriate times in the review process, it is also desirable to solicit input from external experts, sponsors, and users. The process of obtaining external inputs needs to be defined before starting the project to ensure independence of the review from vested interests and potentially biased perspectives while ensuring that the research team has the information needed to achieve subject matter appropriateness and usefulness of the review.
Form multidisciplinary research team. Once the topic has been defined, the initial step in starting the systematic review process is to form a multidisciplinary research team. The research team is responsible for all of the activities and decisions involved in the conduct of the systematic review and must be free of actual or apparent biases relative to the particular topic area under review. The research team should include systematic review methodologists. In addition, depending on the nature of the topic and how the results will be used, the research team will generally also include, but not be limited to, domain experts (e.g. nutrition scientists), clinicians, epidemiologists, and statisticians. In forming the research team for a nutrition-related topic, it is important to include nutrition scientists and at least 1 scientist with a wide rather than narrow range of views and expertise on the topic under review. A broad-based research team works together to identify search terms, develop an analytic framework, answer technical questions, clarify relationships among related topics, and provide input during the peer review process.
Plan for outside inputs. Outside inputs can enhance the quality and usefulness of the review. However, these inputs need to be carefully managed to avoid the potential introduction, or appearance, of bias and vested interests into the review process. Ideally, this is achieved through a prior definition of the roles and responsibilities of the multidisciplinary research team relative to the outside inputs. In all cases, the outside inputs are advisory in nature with the ultimate decisions related to the conduct and decisions involved in the review solely in the hands of the research team. In those cases where a review project has identified sponsors and/or users, an early consultation among the research team and the sponsors or users to ensure a common understanding of the scope of work and user needs can help to ensure the usefulness of the review. Specific subject matter experts and/or an advisory committee representing a wide range of expertise that also often includes persons with varying perspectives may be convened to provide comment on the analytic framework, research questions, eligibility criteria, and search terms. Finally, the rigor of the review can be enhanced by the use of external peer reviewers for the final draft review.
Develop analytic framework. An analytic framework assists in the synthesis and interpretation of the study results and in some cases serves as a guide for the integration of information from multiple types of data. In general, the framework is developed by the systematic review by a collaborative effort of the domain experts and the methodologists and reviewed and refined by other members of the research team. The analytic framework is used by the systematic review methodologists as they review and summarize the data. It has been used successfully by the U.S. Preventive Services Task Force for many years to help formulate research questions (20). Analytic frameworks provide visual maps outlining specific linkages among the populations of interest, exposures, modifying factors, biological role of a nutrient, and outcomes of interest. These frameworks depict the chain of logic that evidence must support to link the exposure to clinical outcomes and should be identified a priori. Defining these relationships can be helpful in further refining the key questions and study eligibility criteria prior to starting the literature search and in interpreting relevant studies once they are identified. In the case of nutrition, the analytical framework reflects the known biological mechanisms of the nutrient and guides in integrating the various types of information available into a coherent picture. An example of the analytic framework used for a systematic review addressing the area of (n-3) fatty acids and cardiovascular disease is provided (Fig. 1) (21).
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The PICO approach is commonly used to formulate research questions. The acronym PICO stands for population (participants), intervention (or exposure for observational studies), comparator, and outcomes (22). Thoughtfully and unambiguously specifying the parameters for each of these attributes allows for research questions to be created that will yield the intended outcome. Various combinations of these parameters form potentially useful questions. In formulating each question, it is necessary to consider the tradeoffs between the desire for ideal knowledge and the reality of limited data, study designs, and available resources. An example of a question and component parts is "What is the overall 5-y mortality in various populations taking 1 g of fish oil daily compared with those taking a placebo?" (Table 3). Alternately, a different question can be generated by selecting an entry from each of the components of the PICO approach (columns of the table) and applying modifiers of interest. For example, "What is the 5-y overall mortality in general populations taking 1 g of fish oil supplement daily compared with those taking a isocaloric fat placebo?"
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Identify search terms. The list of search terms, developed by the multidisciplinary team, must be adequate in scope to capture all of the relevant literature but narrow enough to avoid capturing so much extraneous literature that an undue burden is placed on the research team. To be comprehensive, multiple databases (e.g. Medline, CAB Abstracts, and Cochrane Library Central) as well as citations of relevant retrieved articles should be searched, supplemented by contributions of domain experts. The number of key search terms used in the 3 example reviews ranged from 33 to 130 (Table 2).
Perform literature search. At this point, the domain experts step back from the review process and the methodologists conduct the literature search and summarize the findings. This division of labor ensures a level of objectivity unencumbered by potential biases of domain experts. Clear documentation of the search strategy used and bibliographic databases searched is an inherent part of a systematic review. It facilitates the ability of other groups to reproduce the systematic reviews, allows comparisons across reviews so users can assess their similarities and differences, and serves as a foundation for an efficient updating of the systematic reviews as new findings emerge. In addition, this documentation also facilitates other uses of a systematic review by clarifying both its breath and boundaries.
Evaluate search results.
Systematic reviews of nutrition topics typically evaluate a diverse body of literature that can be diffuse and voluminous. For this reason, screening abstracts guided by eligibility criteria for potentially relevant articles in a consistent, comprehensive, and efficient manner is critical to the integrity of the systematic review. Once potentially relevant literature is identified, full-text articles are retrieved and reviewed for inclusion on the basis of the predetermined criteria. For one topic, effects of soy on health outcomes (12), the initial literature search yielded 
4800 citations (Table 2). A total of 599 potentially relevant full-text articles were retrieved for further evaluation and 178 articles met the inclusion criteria and were included in the final report. A flow diagram depicting the process of literature evaluation and a rejection log of retrieved full-text articles along with the reasons for exclusion should be provided to enhance transparency.
Construct evidence and summary tables, and extract data. Data need to be extracted that will identify information that is important in evaluating the quality and relevance of a study using nutrient-specific criteria in addition to those criteria commonly used. Nutrient supplement information might include intake/dose, source of supplement and chemical analysis, chemical form, mode of delivery, route and duration of delivery, and measures of prior nutritional status. Additional types of information might include the level of the nutrient in the background diet, method used to estimate intake, analytical methods used to assess nutrient status, and whether a nutrient biomarker or other approach was used to validate the dietary data. An evidence table is a comprehensive compilation of a priori-defined data elements extracted from the primary studies that are judged to be important in the interpretation of the evidence. A summary table is a distillation and synthesis of information from evidence tables. It is typically used to succinctly present study characteristics and results in a report or manuscript to support the interpretation of the evidence addressing a specific question. Although a study will usually be found only once in evidence tables, the same study may appear in multiple summary tables addressing different questions. Construction of evidence and summary tables is critical to ensure that all relevant data are extracted and tabulated in a format that will lend itself to subsequent uses. The actual extraction, depending on the nature of that available, may involve data derived from different types of study designs (observation studies, randomized controlled trials, and animal and in vitro studies). Consistent with the different study designs, the format of evidence and summary tables can be adapted to accommodate the types of relevant information important to extract from the full-text articles. The type of acceptable study design and needed information to be included in evidence and summaries tables must be specified a priori.
Assess methodological quality and applicability of studies. Studies included in a systematic review have different protocols, are conducted with different levels of rigor, and their results are reported in a variety of manners. These variations may be manifested as discrepancies of results across studies. Thus, it is important to assess studies for potential bias due to methodological deficiencies and to assess how variations of study conduct (e.g. population enrollment) may influence the results. A critical appraisal of the studies helps to interpret the effects of methodological and clinical/biological heterogeneity on the results. Certain features of study design and conduct such as randomization and blinding in randomized controlled trials, when poorly executed, could result in biased estimates. The effect of these factors, however, is difficult to predict in a specific study (23). Thus, although critical appraisal of studies is guided by certain principles, there are some inevitable subjective components that reviewers and readers should be aware of. Numerous approaches to appraise evidence have been proposed emphasizing different aspects of study design, conduct, and reporting (24). An example of the assessment of methodological quality and applicability of individual studies is depicted (Table 4). The Cochrane Collaboration (25) and the U.S. Preventive Services Task Force (26) and an international group, the Grading Recommendations Assessment, Development and Evaluation working group (27), propose a next step, which is to rate the overall strength of the body of evidence. This step integrates an estimation of the overall risk of bias of evidence based on methodologic study quality as described above with estimations of the directness, consistency, and precision of the evidence. Rating the applicability of the evidence to the target population is also done at this step. The applicability of these approaches to nutrition has not as yet been evaluated.
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Synthesize results. It bears remembering that answers obtained from systematic reviews address only the identified questions. Users of the systematic review (e.g. government agencies, expert panels) must then integrate results from the systematic review with other information to form their practice recommendations or public policies. Sometimes a systematic review may find no or only poor quality evidence or identify inconsistencies among study results. These data would suggest areas where future research needs to be conducted.
Unique considerations when conducting nutrition-related systematic reviews
There are a number of issues that need to be factored into systematic reviews of nutrition-related topics that do not normally arise when systematic reviews of pharmaceuticals and related topics are conducted. These should in no way hamper the process. However, information relative to these issues often need to be captured in systematic reviews to facilitate interpretation of study results and the overall quality, applicability, and strength of the evidence. By accounting for them, their potential influence can be factored into the review.
Baseline exposure. In contrast to pharmaceutical trials, in nutrition-related studies, for the most part all persons have some level of background dietary exposure to the nutrient of interest, either from food and/or supplement intake or, in certain cases, endogenous synthesis (e.g. vitamin D, vitamin K). Background levels of exposures can be difficult to accurately determine due to limitations in currently available assessment methodologies of food intake, incomplete nutrient databases with which nutrient intake estimates are calculated, and temporal changes in exposure. Therefore, information on background intakes and the methodologies used to assess them should be captured in the systematic review so that this level of uncertainty can be factored into data interpretation.
Nutrient status. Nutrient status of an individual or population can affect the response to nutrient supplementation. An accurate approach to evaluate nutrient status is unique to each nutrient and dependent on the availability of nutrient-specific tissue for sampling and homoeostatic mechanisms regulating plasma concentrations via storage depot accretion and release. For some nutrients, a relatively good assessment of nurture can be made; in other cases, the level of uncertainty of nurture is great because of uncertainties about the biological interpretation and/or methodological errors in measuring the indicator of interest that it is necessary to incorporate this information into the systematic review conclusions to facilitate appropriate data interpretation.
Bioequivalence of different chemical forms of nutrients. Many nutrients occur in multiple forms that differ in biological activity. The general approach to address this issue is to calculate nutrient equivalents as was done when setting the recommended dietary allowances for vitamin A (preformed vitamin A, carotenoids), folate (folate, folic acid), vitamin K (phylloquinone and menaquinone), and niacin (preformed niacin, tryptophan) (29–31). The challenge of determining accurate conversion factors for the calculation of nutrient equivalents has recently been demonstrated for β-carotene (29). Capturing information on nutrient forms of baseline diets and intervention products in summarized studies is therefore often essential for appropriate data interpretation.
Bioavailability of nutrients. There are a number of factors that can alter the bioavailability of individual nutrients. These differences must be considered when estimating dietary intake and comparing response to dietary supplementation. Briefly, these include the chemical form of a nutrient (e.g. heme and nonheme iron), nutrient/nutrient interactions (e.g. vitamin C and nonheme iron), nutrient/drug interactions (e.g. isoniazid and vitamin B-6; coumadin and vitamin K; folate and metformin), nutrient/food interactions (e.g. fat-soluble vitamins and dietary fat, zinc- and phytic acid/oxalic acid-containing foods), form of inorganic mineral (e.g. calcium carbonate, citrate, or malate), biological response to single compared with multiple daily doses (e.g. calcium), and habitual intake effect on efficiency of absorption and excretion (e.g. iron, vitamin C). Other factors that may alter nutrient bioavailability include biological status (e.g. iron and pregnancy, achlorhydria and vitamin B-12), food processing (e.g. particle size and dietary fiber; lye-treated corn and trytophan; heat treatment and carotenoids), and, for dietary supplements, factors that alter completeness or rate of release (e.g. coatings, excipients, and surfactants). Bioavailability also differs among nutrients from biological stores. For example, vitamin A has a relatively high bioavailability from liver only when protein status is adequate. Release and deposition of nutrients from storage depots can be unrelated to biological needs. For example, fat-soluble vitamin deposition or release from adipose tissue is altered by weight gain or loss, respectively. Again, capturing relevant information on baseline diet and intervention product bioavailability may be necessary for interpreting summarized results included in a systematic review.
Multiple and interrelated biological functions of a nutrient. Most nutrients have multiple biological functions. A critical point during the research question(s) development and refinement phase of the systematic review process is to clearly define the nutrient-specific scope of the review. This often entails narrowing the range of the work. Some biological functions of nutrients are dependent on multiple nutrients (e.g. folate, vitamin B-12, and vitamin B-6; vitamin D and calcium). These relationships must be defined early in the review process and putative factors incorporated into formulating the questions.
Undefined nature of nutrient intervention. Food-based nutrient interventions, in contrast to nutrient supplement-based interventions, present unique challenges in accurately quantifying the absolute change in intake. For example, one approach to increasing very long-chain (n-3) fatty acid [eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA)] intake is to instruct study subjects to increase fish intake. However, there is considerable variability in the levels of EPA and DHA in different fish, within species of fish (32), time of year the fish were caught, and animal husbandry practices for farm-raised fish. Similarly, assessing EPA and DHA intakes from nutrient supplement data is not without challenges due to the wide variability in fatty acid contents of available fish oil supplements and potential changes in supplement potency during prolonged storage or exposure to heat. Documentation of nutrient intake assessment is important to record.
Uncertainties in assessing dose-response relationships. Measurement and assay procedures can alter apparent dose-response relationships between nutrient intake or dietary pattern and health outcomes. This can be particularly important for systematic reviews where absolute intake/response relationships rather than relative intake response relationships are needed to assess the public health importance of a particular intervention or to identify dose-response relationships to inform the establishment of recommendations. In general, dietary intake methodologies underestimate energy and protein intakes with greater biases for food frequency than 24-h recall methodologies (33). Potential biases for other nutrient intake estimates are not adequately documented but likely exist. Assay procedures for biomarkers of nutritional status can also significantly affect the mean and distribution of reported values and need to be factored into data interpretation (34,35).
Strengths and limitations of systematic review approach for nutrition applications. The systematic review approach brings a number of strengths to the evaluation of evidence in nutrition applications. One of the most compelling strengths is the transparent, objective, and rigorous nature of the process. A clearly defined and unambiguous system is put in place to define the scope of the review, refine the question(s) to be addressed, and identify and select studies prior to reviewing the data. Evidence available to address each question is summarized and critically appraised. This transparency is particularly critical when the systematic reviews are subsequently used by expert panels in developing program or policy guidelines and recommendations.
The ability to combine small studies with meta-analyses increases the statistical power available to address specific questions. This is particularly useful for systematic reviews of nutrition topics where the availability of large trials is relatively limited or lacking. Meta-analyses may be potentially useful in simulating dose-response curves across intervention studies that individually evaluate only 1 or 2 intake levels.
Inherent in the systematic review process is its flexibility in addressing wide variations in the nature of the questions of interest and available amounts and types of data to answer them, while simultaneously ensuring a consistency among topics. This has been particularly challenging for the nutrition community, because the scope of issues has gone beyond those traditionally addressed (from making recommendations for preventing deficiency to minimizing risk of developing chronic disease or nutrient excess). The methodologies of systematic reviews ensure an objective assessment of the available body of literature and minimize biases often encountered in narrative reviews.
When systematic reviews are conducted for the purpose of informing policy and program decisions, an important by-product of a systematic review is the identification of gaps in available data. This information can be used to assist the formulation of research agenda and funding priorities. Equally important is the ability of systematic reviews to identify needed improvements in the quality and nature of reporting. For example, a commonly identified problem in nutrition-related systematic reviews has been that even for topics for which there are a number of published trials, incomplete reporting of basic study design and conduct, as well as poor characterizations of baseline, placebo, and intervention characteristics limits the ability to make definitive conclusions about the outcome of interest. To avoid commonly observed study documentation deficiencies, consolidated standards of reporting trials guidelines for the reporting of randomized trials (16,17) and trials of complex herbal interactions (36) have been proposed. Their use by publishers of nutrition studies is encouraged.
Lastly, the detailed documenting of search strategies and summarizing of the data associated with generating systematic reviews facilitates the updating/revising process as new data become available by providing a comprehensive foundation on which to build. This has the benefits of maximizing the use of limited resources and decreasing the time necessary for generating topic updates.
Notwithstanding these strengths, there are clear limitations of using the systematic review approach in the field of nutrition. By definition, the systematic review process is most effective when limited to addressing targeted questions of limited scope. This may include the population of interest (e.g. age, sex, health status), intervention, comparator, outcome measure, and duration of intervention. Questions that require a broad-based exploratory search approach would better be served by using the systematic review approach after an initial literature search has been conducted and domain experts have narrowed and refined the questions of interest.
Systematic reviews are limited by the quality and availability of data. No approach to analyzing the data can adjust for poor study design, missing data, or publication bias in the area of interest. Multiple systematic reviews addressing what appear to be the same topic can result in different conclusions, causing considerable confusion (37,38). For the most part, discordant results are due to differences in study inclusion and/or exclusion criteria, temporal evolution of available data, and subtle differences in the actual questions addressed that are not initially obvious. By clearly documenting review decisions, comparisons of different reviews can be made and the reasons for differences become apparent.
Using the systemic review process when applied to the field of nutrition allows for considerable flexibility with regard to the types of questions evaluated, studies included, and information captured, as well as the nature of summary statements. Confidence in the results of systematic reviews occurs at a number of levels. These include the transparent nature of the process and involvement of a broad-based research team free of potential biases and vested interests. Confidence also derives from the involvement of trained systematic review methodologists, and, a priori formulation of key questions, search criteria, study evaluation criteria, and information captured for evidence tables, and a priori procedures for obtaining appropriate outside inputs from subject matter experts, sponsors and users while precluding the potential biases and conflicts of interest. Within these boundaries, the conclusions are comprehensive in nature and objective in the assessment of the available information without exceeding the limits of the data. The recognition of a number of challenges not necessarily encountered in other disciplinary areas can enhance the quality and usefulness of nutrition-related systematic reviews. Lastly, it is important to keep in mind that systematic reviews are a tool to be used by expert panels, funding agencies, and other groups and cannot serve as a replacement for expert deliberations and organizational policy development. Users of systemic reviews often need to augment the reviews with other sources of information and where uncertainties exist, with the application of expert scientific judgment. Systematic reviews are a valuable and independent component, but not the end, to decision-making processes by groups responsible for developing science-based recommendations and policies.
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FOOTNOTES |
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2 Author disclosures: A. Lichtenstein, E. Yetley, and J. Lau, no conflicts of interest.
Manuscript received 30 July 2008. Initial review completed 4 September 2008. Revision accepted 17 September 2008.
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LITERATURE CITED |
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TOPABSTRACTIntroductionLITERATURE CITED |
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