"QUIK CHEK"[tw])) NOT ((therapy[ti] OR treatment[ti] OR treat*[ti]) NOT (diagnosis[ti] OR
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1 Supporting information Appendix 1: Search strategy Pubmed (("Clostridium Infections/diagnosis"[majr] AND "Clostridium difficile"[majr]) OR (((("Clostridium difficile"[majr] OR "Clostridium Difficile"[ti]) AND ("Clostridium Infections"[majr] OR "Clostridium Infections"[ti] OR "Clostridium Infection"[ti])) OR "difficile infections"[ti] OR "difficile infection"[ti]) AND ("Biological Assay"[majr] OR "assay"[ti] OR "assays"[ti] OR "stool"[ti] OR "Feces"[majr] OR "feces"[ti] OR "faeces"[ti] OR "test"[ti] OR "tests"[ti] OR "testing"[ti] OR "diagnosis"[ti] OR "Diagnosis"[majr:noexp] OR "Clinical Laboratory Techniques"[majr] OR "diagnostic"[ti] OR "Diagnostic Tests, Routine"[majr] OR "EIA"[ti] OR "Immunoenzyme Techniques"[majr] OR "Immunoassay"[majr] OR "immunoassays"[ti] OR "immunoassays"[ti] OR "cytotoxicity assay"[ti] OR "cytotoxicity assays"[ti] OR "cytotoxicity"[ti] OR "Culture Techniques"[majr] OR "Clinical Laboratory Techniques"[majr] OR "Cells, Cultured"[majr] OR culture[ti] OR cultured[ti] OR "PCR"[ti] OR "Polymerase Chain Reaction"[majr] OR "Polymerase Chain Reaction"[ti] OR "Nucleic Acid Amplification Techniques"[majr] OR "Nucleic Acid Amplification"[ti] OR "RNA Amplification"[ti] OR "DNA Amplification"[ti] OR "Ligase Chain Reaction"[ti] OR "Amplified Fragment Length Polymorphism Analysis"[ti] OR "Multiplex Polymerase Chain Reaction"[ti] OR "Primed In Situ Labeling"[ti] OR "Random Amplified Polymorphic DNA Technique"[ti] OR "Self-Sustained Sequence Replication"[ti] OR "loop-mediated isothermal amplification"[ti] OR "helicase dependent amplification"[ti] OR "chemiluminescent immunoassay"[ti] OR "C.DIFF CHEK-60"[tw] OR "C.DIFF QUIK CHEK"[tw] OR "Immunocard"[tw] OR "Premier toxin A and B"[tw] OR "toxa/b II"[tw] OR "ProSpecT"[tw] OR "GA clostridium difficile antigen"[tw] OR "Vidas"[tw] OR "Xpect"[tw] OR "Tox A/B Quik Chek"[tw] OR "GeneOhm C diff"[tw] OR "BD MAX Cdiff"[tw] OR "Progastro"[tw] OR "Xpert"[tw] OR "GeneXpert"[tw] OR "Illumigene"[tw] OR "Verigene"[tw] OR "Amplivue"[tw] OR "GenomEra"[tw] OR "AdvanSure"[tw] OR "Simplexa"[tw] OR "Seegene"[tw] OR "GenoType CDiff"[tw] OR CHEK-60[tw] OR Premier toxin[tw] OR Premier toxin B[tw] OR toxab[tw] OR GA[tw] OR GeneOhm[tw] OR GenoType[tw] OR "QUIK CHEK"[tw])) NOT ((therapy[ti] OR treatment[ti] OR treat*[ti]) NOT (diagnosis[ti] OR diagnostic[ti])) AND ("2009/01/01"[PDAT] : "3000/12/31"[PDAT])) OR (("Clostridium difficile"[ti] AND ("Biological Assay"[majr] OR "assay"[ti] OR "assays"[ti] OR "stool"[ti] OR "Feces"[majr] OR "feces"[ti] OR "faeces"[ti] OR "test"[ti] OR "tests"[ti] OR "testing"[ti] OR "diagnosis"[ti] OR "Diagnosis"[majr:noexp] OR "Clinical Laboratory Techniques"[majr] OR "diagnostic"[ti] OR "Diagnostic Tests, Routine"[majr] OR "EIA"[ti] OR "Immunoenzyme Techniques"[majr] OR "Immunoassay"[majr] OR "immunoassays"[ti] OR "immunoassays"[ti] OR "cytotoxicity assay"[ti] OR "cytotoxicity assays"[ti] OR "cytotoxicity"[ti] OR "Culture Techniques"[majr] OR "Clinical Laboratory Techniques"[majr] OR "Cells, Cultured"[majr] OR culture[ti] OR cultured[ti] OR "PCR"[ti] OR "Polymerase Chain Reaction"[majr] OR "Polymerase Chain Reaction"[ti] OR "Nucleic Acid Amplification Techniques"[majr] OR "Nucleic Acid Amplification"[ti] OR "RNA Amplification"[ti] OR "DNA Amplification"[ti] OR "Ligase Chain Reaction"[ti] OR "Amplified Fragment Length Polymorphism Analysis"[ti] OR "Multiplex Polymerase Chain Reaction"[ti] OR "Primed In Situ Labeling"[ti] OR "Random Amplified Polymorphic DNA Technique"[ti] OR "Self-Sustained Sequence Replication"[ti] OR "loop-mediated isothermal amplification"[ti] OR "helicase dependent amplification"[ti] OR "chemiluminescent immunoassay"[ti] OR "C.DIFF CHEK-60"[tw] OR "C.DIFF QUIK CHEK"[tw] OR "Immunocard"[tw] OR "Premier toxin A and B"[tw] OR "toxa/b II"[tw] OR "ProSpecT"[tw] OR "GA clostridium difficile antigen"[tw] OR "Vidas"[tw] OR "Xpect"[tw] OR "Tox A/B Quik Chek"[tw] OR "GeneOhm C diff"[tw] OR "BD MAX Cdiff"[tw] OR "Progastro"[tw] OR "Xpert"[tw] OR "GeneXpert"[tw] OR "Illumigene"[tw] OR "Verigene"[tw] OR "Amplivue"[tw] OR "GenomEra"[tw] OR "AdvanSure"[tw] OR "Simplexa"[tw] OR "Seegene"[tw] OR "GenoType CDiff"[tw] OR CHEK-60[tw] OR Premier toxin[tw] OR Premier toxin B[tw] OR toxab[tw] OR GA[tw] OR GeneOhm[tw] OR GenoType[tw] OR "QUIK CHEK"[tw])) NOT ((therapy[ti] OR treatment[ti] OR treat*[ti]) NOT (diagnosis[ti] OR diagnostic[ti])) AND ("2009/01/01"[PDAT] : "3000/12/31"[PDAT])) NOT (("Animals"[mesh] NOT "Humans"[mesh]) OR Editorial[ptyp] OR Case Reports[ptyp] OR comment[ptyp]) AND (english[la] OR dutch[la])
2 Web of science TI=("clostridium difficile" OR "c. diff" OR "c. difficile") AND TI=(assay* OR immunoassay* OR cytotoxic* OR "Polymerase Chain Reaction" OR EIA OR "cell culture*" OR "cultured cell*" OR "PCR" OR "Polymerase Chain Reaction" OR "Nucleic Acid Amplification" OR "RNA Amplification" OR "DNA Amplification" OR "Ligase Chain Reaction" OR "Amplified Fragment Length Polymorphism Analysis" OR "Multiplex Polymerase Chain Reaction" OR "Primed In Situ Labeling" OR "Random Amplified Polymorphic DNA Technique" OR "Self-Sustained Sequence Replication" OR "loop-mediated isothermal amplification" OR "helicase dependent amplification" OR "chemiluminescent immunoassay" OR "repeated" OR "C.DIFF CHEK-60" OR "C.DIFF QUIK CHEK" OR "Immunocard" OR "Premier toxin A and B" OR "toxa/b II" OR " ProSpecT" OR "GA clostridium difficile antigen" OR " Vidas" OR "Xpect" OR "Tox A/B Quik Chek" OR "GeneOhm C diff" OR "BD MAX Cdiff" OR "Progastro" OR "Xpert" OR "GeneXpert" OR "Illumigene" OR "Verigene" OR "Amplivue" OR "GenomEra" OR "AdvanSure" OR "Simplexa" OR "Seegene" OR "GenoType CDiff" OR "CHEK-60" OR "Premier toxin" OR "Premier toxin B" OR "toxab" OR "GA" OR "GeneOhm" OR "GenoType" OR (detection AND (stool OR feces OR faeces OR feces OR faeces)) OR ((test OR tests) AND (diagnos* OR detect*))) NOT TI=(ribotype 027 OR ribotype 078 OR ribotype 017) Cochrane ((clostridium difficile OR "c. diff" OR "c. difficile") AND (assay* OR assay OR assays OR immunoassay* OR immunoassay OR immunoassays OR cytotoxic* OR cytotoxicity OR Polymerase Chain Reaction OR EIA OR cell culture OR cultured cells OR PCR OR "PCR" OR "Polymerase Chain Reaction" OR "Polymerase Chain Reaction" OR "Nucleic Acid Amplification Techniques" OR "Nucleic Acid Amplification" OR "RNA Amplification" OR "DNA Amplification" OR "Ligase Chain Reaction" OR "Amplified Fragment Length Polymorphism Analysis" OR "Multiplex Polymerase Chain Reaction" OR "Primed In Situ Labeling" OR "Random Amplified Polymorphic DNA Technique" OR "Self-Sustained Sequence Replication" OR "loop-mediated isothermal amplification" OR "helicase dependent amplification" OR "chemiluminescent immunoassay" OR repeated OR "C.DIFF CHEK-60" OR "C.DIFF QUIK CHEK" OR "Immunocard" OR "Premier toxin A and B" OR "toxa/b II" OR " ProSpecT" OR "GA clostridium difficile antigen" OR " Vidas" OR "Xpect" OR "Tox A/B Quik Chek" OR "GeneOhm C diff" OR "BD MAX Cdiff" OR "Progastro" OR "Xpert" OR "GeneXpert" OR "Illumigene" OR "Verigene" OR "Amplivue" OR "GenomEra" OR "AdvanSure" OR "Simplexa" OR "Seegene" OR "GenoType CDiff" OR "CHEK-60" OR "Premier toxin" OR "Premier toxin B" OR "toxab" OR "GA" OR "GeneOhm" OR "GenoType" OR ((detection OR detect* OR diagnosis OR diagnost*) AND (stool OR feces OR faeces OR feces OR faeces)) OR ((test OR tests) AND (diagnos* OR detect*)))) OR ((clostridium difficile OR "c. diff" OR "c. difficile") AND (detect* OR diagnos*)) Central ((clostridium difficile OR "c. diff" OR "c. difficile") AND (assay* OR assay OR assays OR immunoassay* OR immunoassay OR immunoassays OR cytotoxic* OR cytotoxicity OR Polymerase Chain Reaction OR EIA OR cell culture OR cultured cells OR PCR OR "PCR" OR "Polymerase Chain Reaction" OR "Polymerase Chain Reaction" OR "Nucleic Acid Amplification Techniques" OR "Nucleic Acid Amplification" OR "RNA Amplification" OR "DNA Amplification" OR "Ligase Chain Reaction" OR "Amplified Fragment Length Polymorphism Analysis" OR "Multiplex Polymerase Chain Reaction" OR "Primed In Situ Labeling" OR "Random Amplified Polymorphic DNA Technique" OR "Self-Sustained Sequence Replication" OR "loop-mediated isothermal amplification" OR "helicase dependent amplification" OR "chemiluminescent immunoassay" OR repeated OR "C.DIFF CHEK-60" OR "C.DIFF QUIK CHEK" OR "Immunocard" OR "Premier toxin A and B" OR "toxa/b II" OR " ProSpecT" OR "GA clostridium difficile antigen" OR " Vidas" OR "Xpect" OR "Tox A/B Quik Chek" OR "GeneOhm C diff" OR "BD MAX Cdiff" OR "Progastro" OR "Xpert" OR "GeneXpert" OR "Illumigene" OR "Verigene" OR "Amplivue" OR "GenomEra" OR "AdvanSure" OR "Simplexa" OR "Seegene" OR "GenoType CDiff" OR "CHEK-60" OR "Premier toxin" OR "Premier toxin B" OR "toxab" OR "GA" OR "GeneOhm" OR "GenoType" OR ((detection OR detect* OR diagnosis OR diagnost*) AND (stool OR feces OR faeces OR feces OR faeces)) OR ((test OR tests) AND (diagnos* OR detect*)))) OR ((clostridium difficile OR "c. diff" OR "c. difficile") AND (detect* OR diagnos*))
3 EMBASE (*clostridium difficile/ OR clostridium difficile.ti OR "c. diff".ti OR "c. difficile".ti) AND (*bacterium identification/ OR exp *assay/ OR exp *cytotoxicity/ OR exp *Polymerase Chain Reaction/ OR *Nucleic Acid Amplification/ OR "Nucleic Acid Amplification".ti OR "RNA Amplification".ti OR exp *Gene amplification/ OR "DNA Amplification".ti OR "Ligase Chain Reaction".ti OR "Amplified Fragment Length Polymorphism Analysis".ti OR "Multiplex Polymerase Chain Reaction".ti OR "Primed In Situ Labeling".ti OR "Random Amplified Polymorphic DNA Technique".ti OR "Self-Sustained Sequence Replication".ti OR "loop-mediated isothermal amplification".ti OR "helicase dependent amplification".ti OR "chemiluminescent immunoassay".ti OR "C.DIFF CHEK-60".mp OR "C.DIFF QUIK CHEK".mp OR "Immunocard".mp OR "Premier toxin A and B".mp OR "toxa/b II".mp OR " ProSpecT".mp OR "GA clostridium difficile antigen".mp OR " Vidas".mp OR "Xpect".mp OR "Tox A/B Quik Chek".mp OR "GeneOhm C diff".mp OR "BD MAX Cdiff".mp OR "Progastro".mp OR "Xpert".mp OR "GeneXpert".mp OR "Illumigene".mp OR "Verigene".mp OR "Amplivue".mp OR "GenomEra".mp OR "AdvanSure".mp OR "Simplexa".mp OR "Seegene".mp OR "GenoType CDiff".mp OR CHEK- 60.mp OR Premier toxin.mp OR Premier toxin B.mp OR toxab.mp OR GA.mp OR GeneOhm.mp OR GenoType.mp OR exp *"diagnosis, measurement and analysis"/ OR EIA.ti OR immunoassay*.ti OR assay*.ti OR cytotoxic*.ti OR cell culture*.ti OR cultured cell*.ti OR PCR.ti OR Polymerase Chain Reaction.ti OR repeated.ti OR repeated test*.mp OR ((test OR tests) AND (diagnos* OR detect*)).ti)
4 Appendix 2: Data extraction form A. Faeces samples Age Consistency Suspicion Clear explanation for the numbers of specimens tested: Repeat specimens from the same patients included? O adults O children O unclear O unformed stools O solid stools O unclear O stools of patients suspected of CDI, namely: o Physician request o Predefined criteria, criteria were: O all unformed stools sent to the laboratory O unclear.... O O No O Unclear B. Index test(s) Name test(s): Manufacturer(s): Type(s): Storage conditions samples: Test executed according to manufacturer s instructions? Ο EIA GDH manual assay read by spectrophotometer Ο EIA GDH manual assay read by eye Ο EIA GDH Membrane assay Ο EIA tox A/B manual assay read by spectrophotometer Ο EIA tox A/B manual assay read by eye Ο EIA tox A/B Membrane assay Ο EIA tox A/B automated assay Ο NAAT Ο Ο No, because:
5 C. Reference test(s): O Cytotoxicity assay Type: Storage conditions samples: Ο Commercial Ο In-house Cell line: Dilution: Neutralization: Controls: Ο C. sordelii antitoxin Ο C. difficile antitoxin Ο positive control Ο negative control Ο None AND/OR O Toxigenic culture Storage conditions samples: Culture medium: Ethanol shock: Incubation period: Ο Ο No Identification C. diff: Identification toxigenic status: Ο toxin EIA, name: Ο PCR, name: Ο cytotoxicity assay
6 Test 1 D. Results (after initial testing, unless only data after repeated testing of indeterminate results are presented) Reference test: Index test:.. Index test + Reference test + Reference test Total Sensitivity: Index test Specificity: Total Indeterminate results: Ο No Ο, namely: Ο Unclear Prevalence of CDI in this study (give 2 numbers, one for toxigenic culture and one for CCTA if both were used): CCTA:.. % TC:.. % Test 2 Reference test: Index test: Index test + Reference test + Reference test Total Sensitivity: Index test Specificity: Total Indeterminate results: Ο No Ο, namely: Ο Unclear Prevalence of CDI in this study (give 2 numbers, one for toxigenic culture and one for CCTA if both were used): CCTA:.. % TC:.. % Add further sheets if more than 2 index or reference tests were evaluated
7 Appendix 3: Quality assessment form Were selection criteria (of stool samples) clearly o described? (at least age of patients, consistency of stool samples, suspicion of CDI (y/n)) If toxin EIA measure both toxin A AND toxin B o Was the time period between reference test and index o test short enough to be reasonably sure that the target condition did not change between the two tests? o Unclear (index test and reference test performed on same sample) Were the required storage conditions met? o EIA/PCR: samples stored according to manufacturer s instructions o Unclear CCA: 4 C, if refrigerated at -20 C thawed only once (toxigenic) culture: no specific requirements Was the execution of the reference test described in o sufficient detail to permit replication of the test? (or was a commercial test executed according to the manufacturer s instructions?) Was incubation appropriate? (48hrs for CCA, 48-72hrs o anaerobically for culture) Were the index test results interpreted without knowledge o of the results of the reference test? o Unclear Were the reference test results interpreted without o knowledge of the results of the index test? o Unclear Were uninterpretable/intermediate test results reported? o, explanation: (partly based on QUADAS,
8 Appendix 4: Quality assessment table Selection Storage conditions met? 2 Indeterminate criteria Tox A/B Reference test Incubation results Author Year described? 1 GDH EIA EIA NAAT CCNA (T)C described? 3 appropriate? 4 Blinding? 5 reported? 6 Barkin 2012 partly? + partly? NA + No? Berry 2014 NA NA + partly? NA No? Boer, de 2010 No NA + NA + NA No? No Bruins 2012 No NA + Buchan 2012 NA NA partly? NA + Calderaro 2013 No Carroll 2013 No Eastwood 2009 No Eckert 2014 Fenner 2008 No Hart 2014 Hirvonen 2013 Huang 2009 Jacobs 1996 Jong 2012 No Kawada 2011 No Kim No Kim No Lalande 2011 No Larson 2010 Le Guern 2012 No Leitner 2013 Massey 2003 Mattner 2012 Musher 2007 Noren 2011 Novak-Weekley 2010 NA?? NA? NA NA + NA NA + NA partly? NA NA NA partly? NA + NA NA partly? NA + NA NA + partly? NA? NA NA NA? NA partly? NA NA NA NA + NA partly? partly? NA + NA partly? NA NA? NA NA + NA + partly? NA NA + NA NA + + NA + NA + + NA + NA? NA? NA No NA partly? NA NA? No NA? NA? NA No NA NA?? NA NA partly?? NA + No? No No? No No? No No? No
9 Selection criteria described? 1 Storage conditions met? 2 Tox A/B EIA NAAT CCNA (T)C Reference test described? 3 Incubation appropriate? 4 Blinding? 5 Author Year GDH EIA O'Connor 2001 NA + + NA Ota NA Pancholi 2012 NA NA + + NA Planche /- +/ No Qutub 2011 No + + NA + NA Reller No? NA NA NA + No Reller No?? NA? NA No No Shin No NA? NA NA? Shin NA? NA NA? Shin No NA NA? NA? Shin No NA?? NA? Sloan 2008 No NA partly? NA NA +? No Snell 2004 No + + NA NA + Soh 2014 No NA NA +/- NA + Stamper NA NA + + NA Stamper NA NA + + NA Staneck 1996 No + NA NA + NA Swindells ? +? N/Unclear No Tenover 2010 NA NA? NA + Terhes 2009 No NA NA + + NA No, only 24hrs Ticehurst 2006 No? NA NA? NA No? No Turgeon 2003 partly? NA NA + NA Van den Berg No NA + NA + NA No?? No Van den Berg No NA? NA + NA No?? No Vanpoucke 2001 No NA partly? NA + NA Viala 2012 No NA NA +/- NA +? Walkty 2013? NA? NA? Wren 2009 No?? NA NA? Zheng 2004 No +/- NA NA NA + Indeterminate results reported? 6
10 1 Selection criteria: scored if age of patients, suspicion of CDI, and consistency of stool samples were all described. In all other instances scored No. 2 Storage conditions: scored? if no storage conditions were described, + if samples were stored according to manufacturer's instructions, +/- if storage conditions were not completely described OR partly inadequate OR inadequate for at least 1 index test of the concerning type, - if storage conditions were incorrect 3 Reference test described: scored (for CCNA) if cell line, dilution and type of antitoxin (C. sordelli/c. difficile antitoxin) were all described. Scored (for TC or C) if culture medium, incubation period, incubation time, identification method of C diff and identification of toxigenicity were all described 4 Incubation appropriate: scored if at least 48hrs 5 Blinding: scored if results of the index test were interpreted without knowledge of the results of the reference test or vice versa 6 Indeterminate results: scored if authors reported if there were any indeterminate index test results after initial and/or repeat testing
11 Appendix 5: Pooled estimates of sensitivity and specificity for assays if 4 or more studies evaluating these assays were available Type Index test No. of studies Compared to CCNA Compared to TC Compared to culture Sensitivity (95% Specificity (95% No. of studies Sensitivity (95% Specificity (95% No. of studies Sensitivity (95% Specificity (95% A: Well-type EIA GDH C. diff Chek ( ) 0.91 ( ) ( ) 0.91 ( ) B: Membrane-type EIA GDH Quik Chek complete GDH ( ) 0.98 ( ) C: Well-type EIA toxins A&B Premier toxins A/B ( ) 0.98 ( ) ( ) 0.98 ( ) Clostridium difficile Tox A/B II ( ) 0.98 ( ) D: Membrane-type EIA toxins A&B Quik Chek Complete Tox A/B* ( ) 1.00 ( ) E: Automated EIA toxins A&B VIDAS CDAB ( ) 0.99 ( ) F: NAAT BD GeneOhm ( ) 0.96 ( ) ( ) 0.99 ( ) Illumigene ( ) 0.99 ( ) Xpert ( ) 0.92 ( ) ( ) 0.95 ( ) * Part of an EIA that detects both toxins A/B and GDH.
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