Progress in Using Systematic Reviews of Animal Studies to Improve Translational Research

Carlijn Hooijmans and colleagues discuss developments that might improve the quality and translation of animal research, focusing on the importance of systematic reviews, the role of an international register of animal studies, and cooperation across the scientific community. Please see later in the article for the Editors' Summary

• Publication year

  2013

• Venue

  PLoS Medicine

• Publication date

  2013-07-01

• Fields of study

  Medicine, Environmental Science

• Identifiers
  DOI 10.1371/journal.pmed.1001482PMID 23874162PMCID 3712909
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• Systematic review and meta-analysis of temozolomide in animal models of glioma: was clinical efficacy predicted?

  2013cited by this paper
• Systematic Reviews of Animal Models: Methodology versus Epistemology

  2013cited by this paper
• The Effects of Probiotic Supplementation on Experimental Acute Pancreatitis: A Systematic Review and Meta-Analysis

  2012cited by this paper
• Extrapolating from Animals to Humans

  2012cited by this paper
• The Effects of Long-Term Omega-3 Fatty Acid Supplementation on Cognition and Alzheimer's Pathology in Animal Models of Alzheimer's Disease: A Systematic Review and Meta-Analysis

  2012cited by this paper
• A call for transparent reporting to optimize the predictive value of preclinical research

  2012cited by this paper
• Reducing the Number of Laboratory Animals Used in Tissue Engineering Research by Restricting the Variety of Animal Models. Articular Cartilage Tissue Engineering as a Case Study

  2012cited by this paper
• An initiative to facilitate well-informed decision-making in laboratory animal research: report of the First International Symposium on Systematic Reviews in Laboratory Animal Science

  2012cited by this paper
• Adaptive changes of mesenteric arteries in pregnancy: a meta-analysis.

  2012cited by this paper
• Drug development: Raise standards for preclinical cancer research

  2012cited by this paper
• Animal Research: Reporting in vivo Experiments—The ARRIVE Guidelines

  2011cited by this paper
• Systematic reviews and meta-analyses of preclinical studies: Publication bias in laboratory animal experiments

  2011cited by this paper
• Publication Bias in Reports of Animal Stroke Studies Leads to Major Overstatement of Efficacy

  2010cited by this paper
• A Gold Standard Publication Checklist to Improve the Quality of Animal Studies, to Fully Integrate the Three Rs, and to Make Systematic Reviews More Feasible

  2010cited by this paper
• Lost in translation: bumps in the road between bench and bedside.

  2010cited by this paper
• Therapeutic Hypothermia for Acute Ischemic Stroke: Ready to Start Large Randomized Trials?

  2010cited by this paper
• Factors Affecting the Apparent Efficacy and Safety of Tissue Plasminogen Activator in Thrombotic Occlusion Models of Stroke: Systematic Review and Meta-Analysis

  2010cited by this paper
• Survey of the Quality of Experimental Design, Statistical Analysis and Reporting of Research Using Animals

  2009cited by this paper
• Why animal studies are often poor predictors of human reactions to exposure

  2009cited by this paper
• Editorial 37(1):MasterEditorial.qxd.qxd

  2009cited by this paper
• Evidence for the Efficacy of NXY-059 in Experimental Focal Cerebral Ischaemia Is Confounded by Study Quality

  2008cited by this paper
• Exercise and menstrual function

  2007cited by this paper
• Translation of research evidence from animals to humans.

  2006cited by this paper
• Establishing risk of human experimentation with drugs: lessons from TGN1412.

  2006cited by this paper
• Methodological quality of systematic reviews of animal studies: a survey of reviews of basic research

  2006cited by this paper
• Comparison of treatment effects between animal experiments and clinical trials: systematic review

  2006cited by this paper
• Evolution and Translation of Research Findings: From Bench to Where?

  2006cited by this paper
• The ethics of research involving animals

  2005cited by this paper
• The Ethics of Research Involving Animals: A Review of the Nuffield Council on Bioethics Report from an Antivivisectionist Perspective

  2005cited by this paper
• The Choice of Animal Model and Reduction

  2004cited by this paper
• Cutting the cost of drug development?

  2004cited by this paper
• Where is the evidence that animal research benefits humans?

  2004cited by this paper
• Emergency medicine animal research: does use of randomization and blinding affect the results?

  2003cited by this paper
• Systematic reviews of animal experiments.

  2002cited by this paper
• Does animal experimentation inform human healthcare? Observations from a systematic review of international animal experiments on fluid resuscitation

  2002cited by this paper
• Nimodipine in Animal Model Experiments of Focal Cerebral Ischemia: A Systematic Review

  2001cited by this paper

• Biological research on mental pain, social pain and other pains not primarily felt in the body: methodological systematic review

  2025cites this paper
• Comparative effectiveness of various administration routes of stem cell therapy and its derivatives for organ inflammation: a systematic review

  2025cites this paper
• EPICYCLE: A confirmatory preclinical study of the anti-rhabdomyosarcoma efficacy of BET bromodomain and cyclin-dependent kinase 9 inhibitors.

  2025cites this paper
• Sleep Deprivation and Memory Consolidation in Rats: A Meta-Analysis of Experimental Studies.

  2025cites this paper
• Does the Use of Methylphenidate Affect Bone Health? A Systematic Review and Meta-analysis of Preclinical Studies

  2025cites this paper
• Experimental methodology used for testing in vivo adhesion of composite meshes for incisional hernia repair: a scoping review

  2025cites this paper
• Role of remote ischaemic conditioning in fracture healing and orthopaedic surgery—a systematic review and narrative synthesis

  2025cites this paper
• Research on the current situation of animal models of abdominal wall hernia in the field of animal experiments: a systematic review of 9098 animals with abdominal wall hernia model

  2025cites this paper
• Efficacy of Nanoparticle-based Localised Immunomodulation to Reduce Graft-versus-host Disease in Murine Model of Bone Marrow Transplantation: A Systematic Review

  2025cites this paper
• A Quantitative Evaluation of the Efficacy of Endochondral Ossification-Based Grafts in Bone Defect Regeneration: An Analysis of Animal Studies.

  2025cites this paper
• Quality, topics, and demographic trends of animal systematic reviews - an umbrella review

  2025cites this paper
• Lessons learned from bovine subclinical endometritis: a systematic review exploring its potential relevance to chronic endometritis in women

  2024cites this paper
• Value of preclinical systematic reviews and meta-analyses in pediatric research

  2024cites this paper
• Biofabrication of biomimetic undulating microtopography at the dermal-epidermal junction and its effects on the growth and differentiation of epidermal cells

  2024cites this paper
• Histological effects of photobiomodulation on delayed tooth replantation: a systematic review

  2024cites this paper
• CRIME-Q—a unifying tool for critical appraisal of methodological (technical) quality, quality of reporting and risk of bias in animal research

  2024cites this paper
• Connecting the dots in neuroscience research: The future of evidence synthesis.

  2024cites this paper
• A Systematic Online Living Evidence Summary of experimental Alzheimer’s disease research

  2024cites this paper
• The effects of flavonoids in experimental sepsis: A systematic review and meta‐analysis

  2023cites this paper
• Gut-on-a-chip models for dissecting the gut microbiology and physiology

  2023cites this paper
• A Systematic Review of the Effect of Cystic Fibrosis Treatments on the Nasal Potential Difference Test in Animals and Humans

  2023cites this paper
• Methodological quality of systematic reviews in dentistry including animal studies: a cross-sectional study

  2023cites this paper
• A systematic mapping review of the evolution of the rat Forced Swim Test: Protocols and outcome parameters.

  2023cites this paper
• Acupoint catgut embedding for simple obesity in animal studies: a systematic review and Meta-analysis.

  2023cites this paper
• Systematic online living evidence summaries: emerging tools to accelerate evidence synthesis

  2023cites this paper
• The role of systematic reviews in identifying the limitations of preclinical animal research, 2000–2022: part 1

  2022cites this paper
• Utilization of sentiment analysis to assess and compare negative finding reporting in veterinary and human literature.

  2022cites this paper
• Phenotypic drug discovery: recent successes, lessons learned and new directions

  2022cites this paper
• A Review on Buckwheat and Its Hypoglycemic Bioactive Components in Food Systems

  2022cites this paper
• Advances in Organ-on-a-Chip Materials and Devices.

  2022cites this paper
• A meta-analytic study of the effects of early maternal separation on cognitive flexibility in rodent offspring

  2022cites this paper
• Black phosphorous-based biomaterials for bone defect regeneration: a systematic review and meta-analysis

  2022cites this paper
• Recommendations to improve use and reporting of statistics in animal experiments

  2022cites this paper
• A methodological review with meta-epidemiological analysis of preclinical systematic reviews with meta-analyses

  2022cites this paper
• Neurodegenerative Diseases Rat models of major neurodegenerative disorders

  2022cites this paper
• A Systematic Review of the Potential Effects of Propolis Extracts on Experimentally-induced Diabetes

  2022cites this paper
• Variability of murine bacterial pneumonia models used to evaluate antimicrobial agents

  2022cites this paper
• Systematic Reviews for Basic Scientists: A Different Beast.

  2022cites this paper
• Effects of Δ9-THC and Type-1 Cannabinoid Receptor Agonists in the Elevated Plus Maze Test of Anxiety: A Systematic Review and Meta-Analysis

  2022cites this paper
• Efficacy of terpenoids in attenuating pulmonary edema in acute lung injury: A meta-analysis of animal studies

  2022cites this paper
• Effects of radiofrequency electromagnetic fields (RF EMF) on cancer in laboratory animal studies.

  2022cites this paper
• Systematic reviews and meta-analyses in animal model research: as necessary, and with similar pros and cons, as in patient research

  2022cites this paper
• Effects of Progesterone on Preclinical Animal Models of Traumatic Brain Injury: Systematic Review and Meta-analysis

  2022cites this paper
• Effect of Acupuncture on Polycystic Ovary Syndrome in Animal Models: Study Protocol for a Systematic Review and Meta-Analysis

  2021cites this paper
• Systematic Reviews

  2021cites this paper
• Validity and Utility of Experimental Animal Models in Perinatal Research

  2021cites this paper
• Libidibia ferrea (jucá) anti-inflammatory action: A systematic review of in vivo and in vitro studies

  2021cites this paper
• A systematic review of neurogenesis in animal models of early brain damage: Implications for cerebral palsy.

  2021cites this paper
• Effects of sleep deprivation on maternal behaviour in animal models: A systematic review and meta‐analysis

  2021cites this paper
• Mining Early Life Risk and Resiliency Factors and Their Influences in Human Populations from PubMed: A Machine Learning Approach to Discover DOHaD Evidence

  2021cites this paper
• Three-Dimensional Co-Culture System of Human Osteoblasts and Osteoclast Precursors from Osteoporotic Patients as an Innovative Model to Study the Role of Nutrients: Focus on Vitamin K2

  2021cites this paper
• A Systematic Review of Therapeutic Approaches Used in Experimental Models of Interstitial Cystitis/Bladder Pain Syndrome

  2021cites this paper
• Quantification of stroke lesion volume using epidural EEG in a cerebral ischaemic rat model

  2021cites this paper
• Does MTA provide a more favourable histological response than other materials in the repair of furcal perforations? A systematic review.

  2021cites this paper
• Systematic Reviews of Animal Studies

  2021cites this paper
• Evaluating the clinical translational relevance of animal models for limbal stem cell deficiency: A systematic review.

  2021cites this paper
• Drivers and Distribution of Henipavirus-Induced Syncytia: What Do We Know?

  2021cites this paper
• Ketogenic diets and the nervous system: a scoping review of neurological outcomes from nutritional ketosis in animal studies

  2021cites this paper
• Quality assessment tools used in systematic reviews of in vitro studies: A systematic review

  2021cites this paper
• Current Status and Limitations of Myocardial Infarction Large Animal Models in Cardiovascular Translational Research

  2021cites this paper
• Efficacy of Alkaloids in Alleviating Myocardial Ischemia-Reperfusion Injury in Rats: A Meta-Analysis of Animal Studies

  2021cites this paper
• Investigating the blood–spinal cord barrier in preclinical models: a systematic review of in vivo imaging techniques

  2021cites this paper
• Renal protective effects of astragaloside IV, in diabetes mellitus kidney damage animal models: A systematic review, meta-analysis.

  2020cites this paper
• THE EFFECT OF MACROPHAGE-TARGETED INTERVENTIONS ON BLOOD PRESSURE - A SYSTEMATIC REVIEW AND META-ANALYSIS OF PRECLINICAL STUDIES.

  2020cites this paper
• Stem Cells as Therapy for Necrotizing Enterocolitis: A Systematic Review and Meta-Analysis of Preclinical Studies

  2020cites this paper
• Can harmonisation of outcomes bridge the translation gap for pre-clinical research? A systematic review of outcomes measured in mouse models of type 2 diabetes

  2020cites this paper
• Biodegradable metals for bone fracture repair in animal models: a systematic review

  2020cites this paper
• Reporting animal research: Explanation and elaboration for the ARRIVE guidelines 2.0

  2020cites this paper
• Importance of Systematic Reviews and Meta-analyses of Animal Studies: Challenges for Animal-to-Human Translation

  2020cites this paper
• Metabolic and behavioural effects of prenatal exposure to non-nutritive sweeteners: A systematic review and meta-analysis of rodent models.

  2020cites this paper
• Can prospective systematic reviews of animal studies improve clinical translation?

  2020cites this paper
• Preclinical Evidence of Probiotics in Colorectal Carcinogenesis: A Systematic Review

  2020cites this paper
• Joining forces: the need to combine science and ethics to address problems of validity and translation in neuropsychiatry research using animal models

  2020cites this paper
• Revisiting the validity of the mouse tail suspension test: Systematic review and meta-analysis of the effects of prototypic antidepressants.

  2020cites this paper
• A Comparison of Osteoblast and Osteoclast In Vitro Co-Culture Models and Their Translation for Preclinical Drug Testing Applications

  2020cites this paper
• Methodological quality (risk of bias) assessment tools for primary and secondary medical studies: what are they and which is better?

  2020cites this paper
• Animal Models and the Search for Drug Treatments for Traumatic Brain Injury

  2020cites this paper
• Similarities and dissimilarities in the effects of benzodiazepines and specific serotonin reuptake inhibitors (SSRIs) in the defensive marble burying test: A systematic review and meta-analysis.

  2020cites this paper
• The intrinsic plasticity of medial vestibular nucleus neurons during vestibular compensation—a systematic review and meta-analysis

  2020cites this paper
• The ARRIVE guidelines 2.0: Updated guidelines for reporting animal research*

  2020cites this paper
• Improving Translation by Identifying Evidence for More Human-Relevant Preclinical Strategies

  2020cites this paper
• Importance of Systematic Reviews and Meta-analyses of Animal Studies: Challenges for Animal-to-Human Translation.

  2020cites this paper
• Prenatal Amino Acid Supplementation to Improve Fetal Growth: A Systematic Review and Meta-Analysis

  2020cites this paper
• A Translational Paradigm to Study the Effects of Uncontrollable Stress in Humans

  2020cites this paper
• Effects on cardiac function, remodeling and inflammation following myocardial ischemia–reperfusion injury or unreperfused myocardial infarction in hypercholesterolemic APOE*3-Leiden mice

  2020cites this paper
• The evidence for the physiological effects of lactate on the cerebral microcirculation: a systematic review

  2019cites this paper
• A systematic review and narrative synthesis on the histological and neurobehavioral long‐term effects of dexmedetomidine

  2019cites this paper
• Efficacy of Terpenoid in Attenuating Aortic Atherosclerosis in Apolipoprotein-E Deficient Mice: A Meta-Analysis of Animal Studies

  2019cites this paper
• Septopremaxillary ligament traction system: a review

  2019cites this paper
• Reporting animal research: Explanation and Elaboration for the ARRIVE guidelines 2019

  2019cites this paper
• Fourier Transform Infrared Spectroscopy of Bone Tissue: Bone Quality Assessment in Preclinical and Clinical Applications of Osteoporosis and Fragility Fracture

  2019cites this paper
• Experimental Aneurysmal Subarachnoid Hemorrhage: Tiding Over

  2019cites this paper
• Minimum Information in In Vivo Research.

  2019cites this paper
• Neuropathic pain after spinal cord injury and physical exercise in animal models: a systematic review and meta-analysis.

  2019cites this paper
• The behavioral phenotype of early life adversity: a 3-level meta-analysis of preclinical studies

  2019cites this paper
• The behavioral phenotype of early life adversity: A 3-level meta-analysis of rodent studies.

  2019cites this paper
• The role of integrin αv and CD44 in GBM migration in human brain

  2019cites this paper
• Are some animal models more equal than others? A case study on the translational value of animal models of efficacy for Alzheimer''s disease.

  2019cites this paper
• Comparison of coated meshes for intraperitoneal placement in animal studies: a systematic review and meta-analysis

  2019cites this paper
• Failure to replicate ? Exacerbated 8-OH-DPAT-induced hypothermia could not be established in single housed mice when tested as part of a battery of depression tests

  2019cites this paper