1College of Life Science and Technology, Heilongjiang Bayi Agricultural University, Daqing, P.R. China;
2Heilongjiang Academy of Agricultural Sciences, Animal Husbandry Research Institute, Harbin, P.R. China
Rice is an important agricultural product consumed globally. Rice polluted by cadmium (Cd) poses serious health risks. Numerous studies have shown that arbuscular mycorrhizal fungi (AMF) decrease Cd concentrations in the grain, shoots, and roots of rice. However, one study showed that AMF increased the root Cd concentration in rice. Therefore, a meta-analysis of the contribution of AMF to rice Cd tolerance became necessary. This meta-analysis was conducted to analyze the role of AMF in Cd tolerance in rice by searching the following databases: ProQuest, PubMed, Scopus, and ScienceDirect. A total of 571 studies were found, of which nine studies and 25 datasets were used in the meta-analysis. The period of inclusion of research reports was from January 1992 to April 2022. The results showed that with the addition of Rhizophagus irregularis, Cd concentration in the roots was higher than in the control group, although the overall Cd concentration in the plant was reduced. Four species of AMF reduced Cd concentration in rice shoots and grain tissues. These AMF species increased the biomass of rice root and shoot tissues; however, they did not affect grain biomass. AMF decreased the transfer factor (TF), and the TF of Glomus versiforme (12.99%) was significantly lower than the other three AMF types. We proposed that Cd could be enriched in rice roots, and the transfer of Cd to the grain could be inhibited. At the time of grain harvesting, rice roots are removed from the soil, thus removing Cd from the soil. This operation can efficiently improve both land-bearing capacity and soil without affecting rice yield. Thus, Cd was enriched in rice roots, and the potential for Cd transfer to the grain was inhibited due to the decreased TF. The future research must focus on how R. irregularis could improve the HMA3 gene expression in rice root, and prevents the transportation of Cd from the roots to shoots.
Key words: absorption, bacteria, rice, pollution, soil
*Corresponding authors: Ruiyong Jing, College of Life Science and Technology, Heilongjiang Bayi Agricultural University, Daqing 163319, P.R. China. Email: [email protected]; and Zhenhua Guo, Heilongjiang Academy of Agricultural Sciences, Animal Husbandry Research Institute. No. 368, Xuefu Road, Harbin 150086, P.R. China. Email: [email protected]
Received: 23 August 2022; Accepted: 17 February 2023; Published: 1 April 2023
© 2023 Codon Publications
This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International (CC BY-NC-SA 4.0). License (http://creativecommons.org/licenses/by-nc-sa/4.0/)
We propose that Cadmium (Cd) can be enriched in rice roots, and the transfer of Cd to grain can be inhibited. When treated with Rhizophagus irregularis, the Cd concentration increased in rice roots; however, the transfer of Cd to the grain could be inhibited.
Rice is an important agricultural product consumed by people globally (Eslami et al., 2015; He et al., 2021; Ma et al., 2021; Sarmast et al., 2021). Cadmium (Cd) pollution is a serious problem that threatens human health and the ecosystem. In the early 20th century, a notorious incident occurred in Toyama, Japan, where Cd accumulation in rice resulted in mass itai-itai disease (Xiao et al., 2020). Our previous report showed that animal manure alters the ecosystem of rice plants (Guo et al., 2022). In fact, at all cultivation stages, from fertilization with animal manure to the cultivation of rice plants, Cd and other heavy metal deposits have been found in all types of crops in farmlands (Majeed et al., 2021). One way to reduce heavy metal-contamination from the soil is to extract heavy metals from the soil using hyperaccumulator plants. In hyperaccumulator plants, shoot Cd reaches 100 mg/kg, and the transfer factor (TF) value is greater than 1 (Jaffre et al., 2013). In China, if the Cd concentration of a farmland is more than 1.0 mg/kg (Luo et al., 2017), the cultivation of crops is forbidden, and the farmland can only be used after improving soil conditions. Scientists have been searching for means to grow food crops that meet certain benchmarks on lands where Cd concentration exceeds these standards.
Arbuscular mycorrhizal fungi (AMF) are a research hotspot in the field of phytoremediation. AMF can regulate Nramp5 and HMA3 gene expressions in rice roots, which are responsible for Cd transport from external soil into root cells (Chen et al., 2019). Research has shown that AMF can increase the growth of hyperaccumulator plants, while a small number of reports have shown that AMF inhibit the growth of hyperaccumulator plants or have no significant effect (Cantamessa et al., 2020; Orlowska et al., 2011). Rice plants are not hyperaccumulators. Most studies have shown that AMF reduce Cd concentration in rice tissues and improve biomass. However, some studies have shown that AMF increase Cd concentration in rice roots (Huang et al., 2018), whereas other studies have shown that there is no significant difference in biomass after AMF are used (Chen et al., 2019; Li et al., 2020). AMF have been found to reduce shoot biomass (Yang et al., 2021). Therefore, a meta-analysis of the role of AMF in Cd tolerance in rice became necessary. The aim of the meta-analysis in this work was to explore the contribution of AMF to Cd tolerance of rice. This study would provide theoretical guidance for utilizing different types of AMF in rice subjected to Cd stress.
A systematic search was performed according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines. Electronic searches of ProQuest, PubMed, Scopus, Web of Sciences, and ScienceDirect databases were conducted. The key terms searched were as follows: (arbuscular mycorrhizal fungi) OR (arbuscular mycorrhizal symbiosis) OR (AM fungi) OR AMF AND (rice OR Oryza sativa L) AND (Cadmium OR Cd). The period of inclusion of research reports was from January 1992 to April 2022. Table 1 lists the inclusion and exclusion criteria used for search in the literature. Randomized controlled trials were not strictly required to be mentioned in the research report, because it was assumed that the planting trials described in the report were randomized trials. Two authors independently completed the literature retrieval, inspection, and inclusion. If the results of the literature inclusion were uncertain, the third author made the final decision.
Table 1. Inclusion and exclusion criteria for meta-analysis.
|Plant included, but not limited to rice||Rice was not used|
|AMF treatment alone or with other treatments of rice||No AMF treatment of rice|
|Cd included||No Cd data|
AMF: arbuscular mycorrhizal fungi; Cd: cadmium.
The retrieved papers were selected one by one according to the entries in the table.
Most of the experimental data were expressed in the form of figures, and specific values could not be found in the paper. Therefore, in the meta-analysis, GetData graph digitizer v2.5 was used to extract specific research data (Zhou et al., 2021). The experimental groups included in the literature were often set up according to different Cd concentrations or for comparisons of the effects of different AMF. Therefore, each dataset group was extracted from the included literature (Maillard and Angers, 2014). All studies included in this meta-analysis contained data expressed as the standard error (SE) or standard deviation (SD). SE was converted to SD before the meta-analysis was conducted.
Each dataset was analyzed as an independent study. Four AMF species were identified: Rhizophagus irregularis, Glomus versiforme, Funneliformis mosseae, and Rhizophagus intraradices. These four AMF species were identified from a subgroup analysis, and the effect of AMF on Cd concentration in rice roots and shoots was analyzed. As there were limited grain data, subgroup analysis was not performed. Then, the effects of AMF on the biomass of rice roots, shoots, and grain under Cd stress were analyzed. According to the continuous model and standard mean difference (SMD), meta-analyses were performed using Stata 12.0 (Stata Corp, College Station, TX, USA). Assessing the heterogeneity I2, if it was greater than 50%, a randomized model was adopted. If the heterogeneity was less than 50%, a fixed model was used. The potential publication bias was also evaluated.
The following equation was used to calculate the average TF:
In the above equation, Croot and Cshoot denote Cd content in rice roots and rice shoots, respectively (Lei et al., 2021). The TF was analyzed with statistical analysis system (SAS) using one-way analysis of variance (ANOVA). Fisher’s protected least-significant difference (LSD) test was used to determine significant differences. P < 0.05 was considered as statistically significant (Guo et al., 2018).
A total of 571 studies were found, of which nine were used for meta-analysis (Chen et al., 2019; Gao et al., 2021; Huang et al., 2018; Lei et al., 2021; Li et al., 2016, 2020; Luo et al., 2017; Yang et al., 2021; Zhu et al., 2022). The nine studies and 25 datasets are shown in Table 2 and Figure 1.
Table 2. Characteristics of the studies included in the analysis.
|Study ID||Dataset No.||AMF||Stage||Seed||Soil Cd||Soil pH||Duration|
|1.||Chen et al., 2019||2||Funneliformis mosseae
|Not mentioned||Upland rice (Hanyou 3)||33 mg/kg||5.8||50 days|
|2.||Gao et al., 2021||1||R. intraradices||Maturity||Upland rice (Hanyou 3)||0.05 mM in water||Not mentioned||105 days|
|3.||Huang et al., 2018||8||F. mosseae
|Not mentioned||Rice (Beidao 4)||0.5, 1, 2, and 5 mg/kg||6.3||90 days|
|4.||Lei et al., 2021||1||Glomus versiforme||Maturity||Upland rice (Hanyou 3)||5 mg/kg||6.23||115 days|
|5.||Li et al., 2016||4||F. mosseae
|Not mentioned||Rice (Zhenghan 9)||0.05 mM and 0.1 mM in water||5.9||60 days|
|6.||Li et al., 2020||4||F. mosseae
|Flowering||Upland rice (Hanyou 3)||2 and 10 mg/kg||5.9||105 days|
|7.||Luo et al., 2017||2||R. intraradices||Ripening||Upland rice (Hanyou 3)||2 and 10 mg/kg||5.8||145 days|
|8.||Yang et al., 2021||2||F. mosseae||Heading
|Upland rice (Hanyou 73)||1.12 mg/kg||7.02||56 days|
|9.||Zhu et al., 2022||1||G. versiforme||Jointing||Upland rice (Hanyou 3)||10 mg/kg||6.23||70 days|
The experimental factors mentioned in each paper that may affect cadmium (Cd) concentrations extracted, and these extracted data were used as the grouping basis for subgroup analysis.
Figure 1. Summary of the study selection procedure.
Most studies showed that treatment with AMF reduced Cd concentration, compared to the control group (Li et al., 2020; Yang et al., 2021). However, when plants were treated with R. irregularis, the plant Cd concentration in roots was higher than that in the control group (SMD = 3.17, 95% confidence interval [CI] = 0.04–6.31, P = 0.05; Figure 2A). AMF Funneliformis mosseae did not affect Cd concentration in roots (SMD = –0.95, 95% CI = –2.24–0.34, P = 0.15; Figure 2A). AMF Glomus versiforme and Rhizophagus intraradices decreased Cd concentration in roots. Overall, 23 datasets showed that AMF reduced Cd concentration in rice roots (SMD = –1.25, 95% CI = –2.24 to –0.26, P = 0.01; Figure 2A). Four species of AMF reduced Cd concentration in rice shoots and grain tissues (Figures 2A and 2B). Figure 2C shows that all articles are distributed on both sides of the midline and are concentrated together, indicating a lack of publication bias. AMF increased the biomass of rice root and shoot tissues (Figure 3A). However, it did not affect the grain biomass (Figure 3B).
Figure 2. Effects of arbuscular mycorrhizal fungi (AMF) treatment on rice cadmium (Cd) concentrations. (A) Forest plot of the roots and shoots.
Figure 2. Effects of arbuscular mycorrhizal fungi (AMF) treatment on rice cadmium (Cd) concentrations. (B) grain, CI = 95%. (C) Funnel plot of root Cd concentration.
Figure 3. Forest plot of arbuscular mycorrhizal fungi (AMF) treatment effects on rice biomass. (A) Roots and shoots; (B) grain, CI = 95%.
AMF decreased TF, indicating that Cd transfer from the roots to shoots was inhibited. The results of the meta-analysis showed that the average TFs of R. irregularis, F. mosseae, R. intraradices, and G. versiforme were 23.63%, 24.77%, 15.01%, and 12.99%, respectively (Figure 4). TF of G. versiforme was significantly lower than that in other three types of AMF.
Figure 4. Effects of four arbuscular mycorrhizal fungi (AMF) treatments on the rice transfer factor (TF).
Rice is an irreplaceable component of the global food supply (Eslami et al., 2015; He et al., 2021; Ma et al., 2021; Sarmast et al., 2021). Cd getting into the food chain through rice poses serious health risks. In particular, Cd in the soil is easily absorbed by rice plants (Kumar et al., 2019). The content of heavy metals in paddy soil is higher than that in dry land soil (Huang et al., 2019). According to the Codex Alimentarius Commission (CAC) of Food and Agriculture Organization (FAO)/World Health Organization (WHO) (CXS 193-1995), the rice grain Cd concentration must be lower than 0.4 mg/kg (Yang et al., 2021). According to farmland standards for Cd concentration in soils (GB 15618-1995) in China, Cd concentration must be lower than 1.0 mg/kg (Luo et al., 2017). Reducing the concentration of Cd in rice has always been a research hotspot (Yan et al., 2019). Two approaches are currently used to address this problem. First, new rice varieties are being created through gene editing. Second, auxiliary agents are added to the cultivated land to reduce the absorption of Cd by rice plants. Both methods can reduce Cd content in rice. However, these methods have disadvantages that can result in reduced Cd absorption but increased arsenic (As) absorption (Li et al., 2022).
Arbuscular mycorrhizal fungi may reduce Cd uptake in rice, kenaf (Hibiscus cannabinus), and maize to produce safer grain varieties (Pan et al., 2022; Yu et al., 2022). One study showed that in the soil with 1.12 mg/kg Cd, adding AMF reduced the rice grain Cd concentration to 0.38 mg/kg (Yang et al., 2021). Another study showed that in the soil with 2 mg/kg Cd, AMF helped to reduce the rice grain Cd concentration by more than 0.4 mg/kg (Luo et al., 2017). This suggested that rice growth could be promoted by the application of AMF only in land with slight Cd pollution. Heavily Cd-polluted land must be improved before it is used safely.
Comparative screening of the AMF currently in use showed that R. irregularis could enrich Cd in rice roots compared to the control group. Moreover, the application of R. irregularis prevented the transfer of Cd from the roots to shoots, reduced Cd concentration in the grain, and did not affect its yield. This suggested that rice could be cultivated on the land that was slightly polluted with Cd. After harvest, the roots and shoots could be removed to reduce Cd content in the soil, thereby improving the soil without affecting the rice yield.
Cadmium in the soil is first absorbed by the rice root system and transferred to the shoots, ultimately accumulating in the grain. IRT1/IRT2, ZIP4, LCT1, YSL, Cd1, Nramp1, and Nramp5 in root apoptosis are transporters that play a crucial role in Cd accumulation in rice (Tang et al., 2017, 2022; Yan et al., 2019; Yang et al., 2021. They can transfer Cd from the soil to rice root tissues. P-type ATPase HMA2 in root tissues transport Cd to the xylem (Yamaji et al., 2013). CAL1 transports Cd in the xylem to the shoots (Luo et al., 2018). In shoot tissues, LCT1 distributes Cd to various organs (Uraguchi et al., 2014). HMA3 in the roots chelates Cd and deposits it in root tissues, preventing its transport to the shoots (Wang et al., 2021). This is similar to the function of AMF in R. irregularis. Currently, no study has directly shown that R. irregularis enhances HMA3 expression in rice roots. However, studies by other groups have shown that F. mosseae and R. intraradices can regulate Nramp5, HMA3, and HMA2 gene expressions (Chen et al., 2019; Yang et al., 2021). Interestingly, under Cd stress, F. mosseae increased the expression of HMA3 whereas R. intraradices inhibited it (Chen et al., 2019) (Figure 5).
Figure 5. Role of arbuscular mycorrhizal fungi (AMF) in absorbing nutrients from the soil.
Arbuscular mycorrhizal fungi have existed for more than 400 million years, coinciding with the settlement of plants on land (Martin et al., 2017). The symbiosis between AMF and plants establishes a pathway for material exchange. The area of AMF mycelia is much larger than that of rice roots, which can help plants absorb mineral nutrients that cannot be obtained from the roots. AMF symbiosis improves plant resistance to pathogens, poor conditions, drought, and pollution (Li et al., 2022). There are many types of AMF, and those with a completed genome sequence include Rhizophagus irregularis (Yildirir et al., 2022), Rhizophagus clarus (Kobayashi et al., 2018), Diversispora epigaea (Sun et al., 2019), Rhizophagus cerebriforme, Rhizophagus diaphanus, and Gigaspora rosea (Morin et al., 2019), Geosiphon pyriformis (Malar et al., 2021), and Gigaspora margarita (Venice et al., 2020). Currently, only R. irregularis, F. mosseae, R. intraradices, and G. versiforme have been applied in research on Cd tolerance in rice. In addition, similar reports have described the use of Glomus mosseae in improving the tolerance of antimony (Sb) pollution in rice (Zhou et al., 2022). Glomus etunicatum, Glomus geosporum, and Glomus Mosseae have been used to increase salt stress tolerance in rice (Tisarum et al., 2020). However, F. mosseae did not decrease Cd concentration in the roots (Chen et al., 2019; Yang et al., 2021).
Whether AMF can promote the uptake of elements that are beneficial to the human body is still unknown. However, some studies have discovered that F. mosseae and G. versiforme can enrich selenium (Se) in rice (Chen et al., 2020), suggesting that AMF not only inhibit the uptake of Cd and manganese (Mn) in rice but also increase the amount of other metals transported by uninhibited transporters. Different types of AMF have different effects (Chen et al., 2019). The meta-analysis results show that the TF of G. versiforme is also low, thus reduces Cd concentration in rice grains.
Significant differences in the Cd accumulation capacity are discovered among different rice varieties (Yan et al., 2019). The collected rice variety data are shown in Table 2. Some studies have determined that the activity of fungi is not affected under flooding conditions (Vallino et al., 2014). Different conditions affect the absorption of Cd by rice. The Cd concentration in rice can also be reduced by switching between drained and undrained conditions (Wang et al., 2020). The lower the soil pH value, the higher the Cd mobility (Zhu et al., 2016). AMF increase the pH value of the soil. By adjusting the pH, AMF reduce the content of inorganic Cd in the soil and increase the amount of residual Cd (Li et al., 2022). In addition, AMF mycelia adsorb large amounts of heavy metals and reduce their entry into plants (Zhang et al., 2009).
Certain limitations were confronted in the research on rice and AMF. For example, agricultural cultivation encompasses a large and complex system that includes tillage, fertilization, crops, the plant rhizosphere microbial environment, and the addition of AMF. Chemical or organic fertilizers are used concurrently during plantation of crops. Our previous research demonstrated that the application of animal manure to the soil changes the original microbial population, resulting in the formation of a new microbial ecology (Guo et al., 2022). Similarly, research by other teams established that under the application of different fertilizers, the biomass of AMF increased along with the biomass of fungal protozoa and nematodes, thereby significantly altering the composition of AMF community (Jiang et al., 2020).
The studies included in this work focused on the extent to which AMF contributed to rice yield and reduced Cd content. These factors did not account for how much AMF was benefited by the rice. In the symbiotic relationship between AMF and plants, AMF obtain fixed carbon resulting from plant photosynthesis, which is approximately 4–20% of the total carbon fixation in a whole plant (Zhang et al., 2022). The roots of plants recruit AMF, and the mycelia of AMF recruit soil microorganisms. The results of a 13C tracer study showed that plant roots provided a carbon source for AMF and that AMF provided a carbon source for soil microorganisms (Zhou et al., 2020). AMF secrete proteins to supply soil microorganisms. R. irregularis secrete SP7, which affects the gene expression of host plants (Kloppholz et al., 2011). In addition to its effects on host plants, AMF-secreted proteins can also manipulate the activities of other microorganisms (Snelders et al., 2020).
Arbuscular mycorrhizal fungi treatment concentration, duration, and soil Cd concentration are shown in Table 2. This study focused on the summary effect of the included data and overlooked the fact that treatment concentrations may have varied from one study to another study. Only publicly published data were collected, while unpublished studies with negative results were not considered. Figure 2C displays a function plot demonstrating no publication bias in the root concentration data. Other sample data could have the probability of including publication bias and sketched data.
Although only discussing the relationship between AMF and rice has limitations, the present authors believed that the experimental design of the included literature followed the following three principles: (1) single-factor analysis; (2) repeated trials; and (3) randomized trials. Therefore, the authors believe that the results of this research are credible.
Achieving a balance between the reasonable cultivation of land and soil improvement has always been a challenge. Although F. mosseae promotes the expression of Nramp5 and HMA3 gene expressions, the results of the meta-analysis showed that F. mosseae did not improve the root Cd concentration. Based on the findings of the analysis, the future studies should focus on R. irregularis, as this AMF can improve HMA3 expression in rice roots. Thus, Cd can be enriched in rice roots, and the transfer of Cd to the grain can be inhibited. Thus, this method can efficiently improve both land-bearing capacity and soil conditions without affecting the yield of rice.
The authors thank Accdon (www.accdon.com) for its linguistic assistance for preparing this manuscript.
This work was supported by the “Three Longitudinal” scientific research support program of Heilongjiang Bayi Agricultural University (ZRCPY202114) and the Daqing Guided Science and Technology Project (zd-2021-78).
The authors declare that they had no conflict of interest to report.
Please contact corresponding authors for data requests.
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|Section/topic||#||Checklist item||Reported on page #|
|Title||1||Identify the report as a systematic review, meta-analysis, or both.||1|
|Structured summary||2||Provide a structured summary including, as applicable: background; objectives; data sources; study eligibility criteria, participants, and interventions; study appraisal and synthesis methods; results; limitations; conclusions and implications of key findings; systematic review registration number.||2|
|Rationale||3||Describe the rationale for the review in the context of what is already known.||4|
|Objectives||4||Provide an explicit statement of questions being addressed with reference to participants, interventions, comparisons, outcomes, and study design (PICOS).||4|
|Protocol and registration||5||Indicate if a review protocol exists, if and where it can be accessed (e.g., Web address), and, if available, provide registration information including registration number.||No|
|Eligibility criteria||6||Specify study characteristics (e.g., PICOS, length of follow-up) and report characteristics (e.g., years considered, language, publication status) used as criteria for eligibility, giving rationale.||5|
|Information sources||7||Describe all information sources (e.g., databases with dates of coverage, contact with study authors to identify additional studies) in the search and date last searched.||5|
|Search||8||Present full electronic search strategy for at least one database, including any limits used, such that it could be repeated.||5|
|Study selection||9||State the process for selecting studies (i.e., screening, eligibility, included in systematic review, and, if applicable, included in the meta-analysis).||6|
|Data collection process||10||Describe method of data extraction from reports (e.g., piloted forms, independently, in duplicate) and any processes for obtaining and confirming data from investigators.||5|
|Data items||11||List and define all variables for which data were sought (e.g., PICOS, funding sources) and any assumptions and simplifications made.||5|
|Risk of bias in individual studies||12||Describe methods used for assessing risk of bias of individual studies (including specification of whether this was done at the study or outcome level), and how this information is to be used in any data synthesis.||5|
|Summary measures||13||State the principal summary measures (e.g., risk ratio, difference in means).||5|
|Synthesis of results||14||Describe the methods of handling data and combining results of studies, if done, including measures of consistency (e.g., I2) for each meta-analysis.||No|
|Risk of bias across studies||15||Specify any assessment of risk of bias that may affect the cumulative evidence (e.g., publication bias, selective reporting within studies).||5|
|Additional analyses||16||Describe methods of additional analyses (e.g., sensitivity or subgroup analyses, meta-regression), if done, indicating which were pre-specified.||5|
|Study selection||17||Give numbers of studies screened, assessed for eligibility, and included in the review, with reasons for exclusions at each stage, ideally with a flow diagram.||6|
|Study characteristics||18||For each study, present characteristics for which data were extracted (e.g., study size, PICOS, follow-up period) and provide the citations.||6|
|Risk of bias within studies||19||Present data on risk of bias of each study and, if available, any outcome level assessment (see item 12).||6|
|Results of individual studies||20||For all outcomes considered (benefits or harms), present, for each study: (a) simple summary data for each intervention group (b) effect estimates and confidence intervals, ideally with a forest plot.||No|
|Synthesis of results||21||Present results of each meta-analysis done, including confidence intervals and measures of consistency.||6|
|Risk of bias across studies||22||Present results of any assessment of risk of bias across studies (see Item 15).||6|
|Additional analysis||23||Give results of additional analyses, if done (e.g., sensitivity or subgroup analyses, meta-regression [see Item 16]).||6|
|Summary of evidence||24||Summarize the main findings including the strength of evidence for each main outcome; consider their relevance to key groups (e.g., healthcare providers, users, and policy makers).||7|
|Limitations||25||Discuss limitations at study and outcome level (e.g., risk of bias), and at review-level (e.g., incomplete retrieval of identified research, reporting bias).||9|
|Conclusions||26||Provide a general interpretation of the results in the context of other evidence, and implications for future research.||10|
|Funding||27||Describe sources of funding for the systematic review and other support (e.g., supply of data); role of funders for the systematic review.||10|
From: Moher D, Liberati A, Tetzlaff J, Altman DG, The PRISMA Group (2009). Preferred Reporting Items for Systematic Reviews and Meta-Analyses: The PRISMA Statement. PLoS Med 6(7): e1000097. doi:10.1371/journal.pmed1000097
For more information, visit: www.prisma-statement.org.