Main Study Findings and Authors’ Conclusions

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Screening of Shiga-toxigenic Escherichia coli in Clinical Fecal Samples: A Review of Diagnostic Accuracy, Clinical Utility, Cost-Effectiveness and Guidelines [Internet]. Ottawa (ON): Canadian Agency for Drugs and Technologies in Health; 2015 Jul 8.

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Screening of Shiga-toxigenic Escherichia coli in Clinical Fecal Samples: A Review of Diagnostic Accuracy, Clinical Utility, Cost-Effectiveness and Guidelines [Internet].

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APPENDIX 5Main Study Findings and Authors’ Conclusions

First
Author,
Publication
Year,
Country

Main Findings and Authors’ Conclusion

Health Technology Assessments (HTA)

ECRI eport,¹⁰
2015,
USA

Main Findings:

Test (using nucleic acid based GPP)	Ref Test	No. of samples	Sensitivity (%)	Specificity (%)	PPA^a (%)	NPA^b (%)
BD Max Enteric Bacterial Panel	Bacterial culture or 2 of 3 multiplex panels	434	NA	NA	100 (25 to 100)	99.5 (98.3 to 99.9)
	Bacterial culture and EIA	3,457	75 (40.9 to 92.9)^c 100 (34.2 to 100)^d	99.3 (98.8 to 99.6)^c 99.0 (98 to 99.5)^d	NA	NA
	National Reference Laboratory	528	100	98.8	NA	NA
FilmArray Gastrointestinal Panel kit	PCR with bidirectional sequencing	1,556	100 (89.4 to 100)	99.7 (99.2 to 99.9)	NA	NA
FTD bacterial gastroenteritis panel	Bacterial culture or 2 of 3 multiplex panels	434	NA	NA	100 (25 to 100)	99.8 (98.7 to 100)
ProGastro SSCS	Bacterial culture and EIA	1,244	100 (63 to 100	99.2 (98 to 100)	NA	NA
RIDA Gene EHEC/EPEC panel	Bacterial culture or 2 of 3 multiplex panels	434	NA	NA	0 (0 to 97.5)	99.5 (98.3 to 99.9)
xTAG GPP	EIA	901	NA	NA	100	99.4
	DNA sequencing	901	NA	NA	100	99.5
	PCR	440	NA	NA	100	99.2
	Bacterial culture and EIA	1,534	100 (20.7 to 100)	98.5 (97.7 to 99.1)	NA	NA
Seeplex Dairrhea ACE detection system	Discrepant analysis^e using bacterial culture or uniplex PCR	245	NA	NA	100	99.6

: EIA = enzyme immunoassay, GPP = gastrointestinal pathogen panel, NA = not applicable, NPA = negative percent agreement, NR = not reported, PCR = polymerase chain reaction, PPA = positive percent agreement
a: Negative percent agreement (NPA) was defined as proportion of patients who received a negative test result on the comparator assay who also received a negative test result on the assay under investigation.
b: Positive percent agreement (PPA) was defined as proportion of patients who received a positive test result on the comparator assay who also received a positive test result on the assay under investigation.
c: preserved and unpreserved samples
d: preserved samples only
e: The authors used a discrepant analysis method in which a sample is positive if both the bacterial culture and the multiplex PCR have positive results or if either the bacterial culture or the multiplex PCR have positive results and a uniplex PCR has positive results.
: Note:
95% confidence limit is inserted within parenthesis.

No studies, investigating if using nucleic acid based GI pathogen panels resulted in improved health outcomes compared with standard diagnostic procedures, were identified.

No cost-effectiveness studies on nucleic acid based GI pathogen panels were identified.

Cost information:
Payment information for nucleic acid based Gastrointestinal Panels (GPP)

Procedure	Number of targets	Clinical laboratory fee schedule (US$, 2015)
Gastrointestinal pathogen detection by nucleic acid of using multiplex reverse transcription and multiplex amplified probe technique	3 to 5	235.92
	6 to 11	392.50
	12 to 25	766.47

Authors’ Conclusion:
The report included a summary of results but no specific conclusions were provided.

Abubakar,⁴
2007,
UK

Main Findings:
Sensitivity of various tests to detect STEC

Test	Reference test	No. of studies	Effect size
Test	Reference test	No. of studies	Minimum	Maximum	Summary estimate
c-PCR (all but 1 study using rt-PCR)	SMAC culture	7	0.89 (0.83 to 0.93)	1.00 (0.70 to 1.00)	NR
PCR (BAX system)	SMAC culture	1	1.00 (0.68 to 1.00)		NA
rt-PCR	c-PCR	2	0.96 (0.94 to 0.98)	1.00 (0.92 to 1.00)	NR
EIA (Premier EHEC)	SMAC culture (or SMAC and cytotoxicity in 1 study)	5	0.82 (0.59 to 0.94)	1.00 (0.51 to 1.00)	0.92 (0.86 to 0.97)
EIA (Premier EHEC)	PCR	1	0.83(0.44 to 0.97)		NA
EIA (several types)^a	SMAC culture	6	0.86 (0.76 to 0.93)	1.00 (0.70 to 1.00)	NR
EIA Verotox F assay	Vero cell phenotyping assay	1	1.00(0.94 to 1.00)		NA
EIA (Duopath Verotoxin)	EIA (Premier EHEC)	1	1.00 (0.92 to 1.00)		NA
EIA (RidaScreen Verotoxin)	c-PCR	1	0.67 (0.53 to 0.79)		NA
RPLA (VTEC screen)	Culture or Vero cell	5	0.89 (0.56 to 0.98)	1.00 (0.51 to 1.00)	0.99 (0.95 to 1.02)

a: Several types of EIA: Premier E. coli O157, LMD laboratories, in-house, ProSpecT assay, ImmunoCard STAT E. coli O157

Specificity of various tests to detect STEC

Test	Reference test	No. of studies	Effect size
Test	Reference test	No. of studies	Minimum	Maximum	Summary estimate
c-PCR ( all but 1 study using rt-PCR)		7	0.92 (0.65 to 0.99)	1.00 (0.76 to 1.00)	NR
PCR (BAX system)	SMAC culture	1	1.00 (0.82 to 1.00)		NA
rt-PCR	c-PCR	2	0.98 (0.95 to 0.99)	1.00 (0.99 to 1.00)	NR
Premier EHEC	SMAC culture	5	0.92 (0.90 to 0.94)	1.00 (0.99 to 1.00)	0.98 (0.97 to 0.99)
EIA (Premier EHEC)	PCR	1	0.82 (0.72 to 0.89)		NA
EIA (several types)^a	SMAC culture	6	0.98 (0.97 to 0.99)	1.00 (0.99 to 1.00)	NR
EIA Verotox F assay	Vero cell phenotyping assay	1	1.00 (0.96 to 1.00)		NA
EIA (Duopath Verotoxin)	EIA (Premier EHEC)	1	1.00 (0.97 to 1.00)		NA
EIA (RidaScreen Verotoxin)	c-PCR	1	0.97 (0.94 to 0.98)		NA
RPLA (VTEC screen)		5	0.67 (0.30 to 0.90)	1.00 (0.89 to 1.00)	0.99 (0.97 to 1.00)

a: Several types of EIA: Premier E. coli O157, LMD laboratories, in-house, ProSpecT assay, ImmunoCard STAT E. coli O157

Cost-effectiveness for detecting E. coli with various strategies Sensitivity Analysis

Strategy	Cost per sample (£)	Cost per case detected (£)
Strategy	Cost per sample (£)	Baseline isolation rate = 0.11%	Lowest isolation rate = 0.01%	Highest isolation rate = 0.51%
Status quo - culture	4.99	5,273.20	56,800.00	1,113.73
Culture replaced by rt-PCR	5.22	5,025.18	54,128.46	1,061.34
Culture replaced by ELISA	5.44	5,405.38	58,223.86	1,141.64
Culture and additional testing by rt-PCR for high-risk patients	5.66	5,306.20	58,623.25	1,149.48
Culture and additional testing by ELISA for high-risk patients	5.44	5,343.75	58,223.86	1,141.64
Culture and additional testing by rt-PCR for all patients for E.coli only	5.89	5,514.38	60,870.64	1,193.54

Authors’ Conclusion:
“Evidence from this systematic review suggests that rapid diagnostic assays, especially PCR, for Salmonella, Campylobacter and E. coli O157 are highly accurate. Less is known about the benefits of testing for toxin-producing pathogens and the significance of additional positives detected by these assays. It is unclear whether the additional benefits derived from early diagnosis and more sensitive detection can justify the large set-up costs of rapid tests, particularly if they remain diagnostic adjuncts to culture. Any decisions regarding the use of these assays must consider the speed of diagnosis (including transportation and reporting delays), effect on clinical outcome and costs of implementation simultaneously.” P.x

Non-randomized studies

Chui,¹⁷
2015,
Canada

Main Findings:

Diagnostic accuracy

Test	Ref Test	Sample size	Sensitivity (%)	Specificity (%)	PPV (%)	NPV (%)
EIA (Shiga Toxin Chek) - stool	NA	784	70.0	99.4	73.7	99.2
EIA (Shiga Toxin Chek) - Broth	NA		80.0	98.2	53.3	99.5
EIA (Shiga Toxin Quik Chek) - stool	NA		70.0	99.9	93.3	99.2
EIA (Shiga Toxin Quik Chek) - broth	NA		85.0	100.0	100.0	99.6
rt-PCR - broth	NA		95.0	100.0	100.0	99.9

Authors’ Conclusion:
“In conclusion, the EIAs evaluated in this study are viable alternatives to amplification assays for frontline microbiology laboratories as a primary screening method for STEC. However, the challenge still remains for the reference laboratories to find a less labor-intensive method to isolate and identify the specific type of non-O157 STEC isolates.” P. 1021

Chiu,¹
2013,
Canada

Main Findings:

Diagnostic accuracy

View in own window
Test Ref
Test Sample
size Sensitivity
(%) Specificity
(%) PPV
(%) NPV
(%)
EIA (IMC; ImmunoCard STAT!) rt-PCR 819 35 99 NR NR

Authors’ Conclusion:
“In a routine clinical microbiology laboratory where molecular diagnostic methods may be unavailable due to a variety of reasons, sensitive enzyme immunoassay or lateral flow devices targeting detection of STEC would be the preferred method for the detection of O157 and non-O157 STEC. The ImmunoCard STAT!® assay was selected for this study mainly due to the ease of performance for a routine microbiology laboratory and dedicated equipment or extensive training is not required. However, real-time PCR or any form of amplification assay remains comparatively and significantly more sensitive than existing immunoassay methods. Until a more sensitive and a less labor-intensive screening method becomes commercially available, real-time PCR remains the most reliable method for clinical laboratories wishing to detect non-O157 STEC from stool specimens.” P. 12

Chui,²⁴
2010,
Canada

Main Findings:

Sensitivity and specificity

Test	Ref Test	Sample size	Sensitivity (%)	Specificity (%)
rt-PCR (TaqMan)	A true positive was defined as a sample that yielded at least 3 positive results for the 5 test methods. A true negative was defined as a sample that yielded at least 3 negative results for the 5 test methods	36 stool samples (Sensitivity and specificity reported for Stx1/Stx2)	100/100	100/100
rt-PCR (HybProbe)			91/96	100/100
rt-PCR (SYBR Green)			100/92	84/100
rt-PCR (LUX)			100/100	100/100
c-PCR			94/96	84/100

: Note: PPV and NPV were not reported

Cost and time requirement of test

View in own window
Test Cost per 25 samples
(C$) Time requirement
rt-PCR (TaqMan) 58.94 3h 30m
rt-PCR (HybProbe) 196.11 2h
rt-PCR (SYBR Green) 73.30 2h 40m
rt-PCR (LUX) 138.08 4h 10m
c-PCR 53.35 4h 10m

Authors’ Conclusion:
“This evaluation concluded that the TaqMan-based probes were most appropriate in high throughput clinical diagnostic laboratories in consideration of cost, turn around time, and assay performance. P. 469

Church,²⁷
2007,
Canada

Main Findings:

Sensitivity and specificity

View in own window
Test Ref Test Sample
size Sensitivity
(%) Specificity
(%) PPV
(%) NPV
(%)
SMAC CHROMagar O157 3,116 96.3 99.96 100 100

Study cost for 3,116 samples assayed by each method

Item	Assay with SMAC agar	Assay with CHROMagar
Cost of medium(C$)	872.48	5,297.20
Cost of other material (C$)	1,223.25	445.04
Total time spent by medical laboratory technologist (h)	220.8	70.1
Total study cost (C$)	10,744.12	8,501.77

Authors’ Comment/Conclusion:
“The improved diagnostic performance and efficiency of CHROM would allow more appropriate management of E.coli O157 cases and outbreaks.” P. 3099

Gerritzen,²²
2011,
Germany

Main Findings:

Diagnostic accuracy

Test	Ref Test	Sample size	Sensitivity (%)	Specificity (%)	PPV (%)	NPV (%)
rt-PCR (direct)	Enriched culture	754	96.4	97.8	NR	NR
EIA (enrichment based test)	Enriched culture	754	76.8	99.4	NR	NR
Vero cell cytotoxicity assay (VCA)	Enriched culture	754	83.9	99.2	NR	NR

Authors’ Conclusion:
“The direct fecal stx real-time PCR proved superior to enrichment based VCA and EIA and can be recommended as a quick and sensitive tool for the early diagnosis of STEC infection in addition to microbiological culture.” P. 993

Gouali,¹⁹
2013,
France

Main Findings:

Diagnostic accuracy

View in own window
Test Ref Test Sample
size Sensitivity
(%) Specificity
(%) PPV
(%) NPV
(%)
CHROMagar STEC Standard (Drigalski agar) 329 91.4 83.7 40 98.8

Authors’ Conclusion:
“In conclusion, the good performance of CHROMagar STEC agar medium, in particular, the high negative predictive value, and its capacity to identify NSF O157:H7 as well as common non-O157 STEC may be useful for clinical bacteriology, public health, and reference laboratories; it could be used in addition to a method targeting Shiga toxins (detection of stx genes by PCR, immunodetection of Shiga toxins in stool specimens, or Vero cell cytotoxicity assay) as an alternative to O157 culture medium. This combined approach should allow rapid visualization of both putative O157 and non-O157 STEC colonies for subsequent characterization, essential for real-time surveillance of STEC infections and investigations of outbreaks.” P. 894

Grif,²⁸
2007,
Austria

Main Findings:

Diagnostic accuracy

Test	Ref Test	Sample size	Sensitivity (%)	Specificity (%)	PPV (%)	NPV (%)
EIA (Premier EHEC ELISA)	PCR	240 (enriched) (145 std method & 95 Mod method)	94.6 (Stx) – Std 96.6 (Stx) -- Mod	96.3 (Stx) – Std 98.5 (Stx) -- Mod	90 (Stx) – Std 97 (Stx) -- Mod	98 (Stx - Std) 98 (Stx) -- Mod
EIA (IMC; DV-test™)	PCR	240 (enriched) (145 std method & 45 modified method)	46.2 (Stx1), 75.0 (Stx2) – Std 80.0 (Stx1), 100.0 (Stx2) - Mod	79.8 (Stx1), 99.1 (Stx2) – Std 81.3 (Stx1), 62.0 (Stx2) - Mod	20 (Stx1), 95 (Stx2) – Std 53 (Stx1), 35 (Stx2)- Mod	93 (Stx1), 94 (Stx2) – Std 94 (Stx1), 100 (Stx2) – Mod

Authors’ Conclusion:
“In conclusion, we found no advantage in the use of the DVtest™ standard protocol for routine screening of human stool samples, with a low sensitivity and specificity and a quite high percentage of equivocal results being observed. The modified protocol of the DV-test™ produced more reliable results for direct screening of clinical human stool samples. However, this method provides no time benefit when compared with the Premier EHEC-ELISA analysis, which has a higher sensitivity and specificity in general. Thus, a rapid screening of clinical human stool samples for the presence of Stx, in particular, Stx2, has still to be developed.” P.98–99

Grys,²⁵
2009,
USA

Main Findings:

Diagnostic accuracy

Test	Ref Test	Sample size	Sensitivity (%)	Specificity (%)	PPV (%)	NPV (%)
rt-PCR	EIA (ProSpecT) and culture CHROMagar O157 & SMAC	289 stool samples (204 prospectively collected consecutive samples submitted to the clinical microbiology laboratory and 85 archived samples)	100 (for all samples and for each subsets)	100 (for all samples and for each subsets)	NR	NR

Authors’ Comment/Conclusion:
“The PCR assay demonstrated 100% sensitivity and specificity compared to EIA and/or culture and more rapid turnaround than either EIA or culture” P. 2008

Hermos,²³
2011,
USA

Main Findings:

Diagnostic accuracy

Test	Ref Test	Sample size	Sensitivity (%)	Specificity (%)	PPV (%)	NPV (%)
SMAC	Culture confirmed by HSLI	5,110 stool samples	58.0 (43.2 to 71.8) - all STEC 87.9 (71.8 to 96.6) - STEC O157:H7	99.9 (99.9 to 100) - all STEC	96.7 (82.8 to 99.9) - all STEC	99.6 (99.4 to 99.7)- all STEC
EIA (Premier EHEC)			96.0 (86.3 to 99.5) - all STEC 93 (79.8 to 99.3) - STEC O157:H7	99.7 (99.5 to 99.8) - all STEC	76.2 (63.8 to 86.0) - all STEC	99.9 (99.9 to 100) - all STEC

Authors’ Conclusion:
“The Premier EHEC assay was significantly more sensitive than SMAC culture for diagnosis of STEC, and O157:H7 and non-O157:H7 STEC caused infections of similar severity in children.” P.955

Mccallum,⁷
2013,
Australia

Main Findings:

Diagnostic accuracy

View in own window
Test Ref
Test Sample
size Sensitivity
(%) Specificity
(%) PPV
(%) NPV
(%)
CHROMagar STEC Easy- Plex MT- PCR 282 stool 50.0 93.1 13.6 98.9
CT-SMAC Easy-Plex MT-PCR 16.7 93.8 5.6 98.0

Authors’ Conclusion:
“The incidence of STEC associated enteritis in Tasmania was almost six times greater than the previously reported Australian average. STEC Screening Easy-Plex MT-PCR was more sensitive than both CHROMagar STEC and CT-SMAC media for the detection of STEC from preenriched faecal samples.” P.681

Monno,¹⁶
2015,
Italy

Main Findings:

Diagnostic accuracy

View in own window
Test Ref Test Sample
size Sensitivity
(%) Specificity
(%) PPV
(%) NPV
(%)
ELISA Molecular method (PCR) 16 fecal samples 100 100 NR NR

Authors’ Conclusion:
“The detection of verotoxin in faecal samples by ELISA is a simple, sensitive, specific and rapid method (2 hours) of considerable utility for routine clinical testing laboratories without access to more specialized diagnostic procedures.” P.1 (preprint)

Navidad,¹⁸
2013,
USA

Main Findings:

Diagnostic accuracy

Test	Ref Test	Sample size	Sensitivity (%)	Specificity (%)	PPV (%)	NPV (%)
GPP-ASR (Luminex xTAG)	SMAC & microscopy for E.Coli O157:H7	254 stool	100 (55 to 100)	100 (95 to 100)	100 (55 to 100)	100 (95 to 100)
GPP-ASR (Luminex xTAG)	EIA & rt-PCR for EHEC/STEC		94 (79 to 99)	100 (98 to 100)	100 (87 to 100)	100 (87 to 100)

Authors’ Conclusion:
“In conclusion, our study determined the performance of the Luminex GPP ASR and demonstrated that it could be suitable as a primary screening tool for enteric bacteria, viruses, and parasites. We also showed that the sensitivity of assays using GPP ASRs was equivalent to or better than that of conventional and molecular test methods currently employed by clinical and public health laboratories” P. 3023

Teel,²⁶
2007,
USA

Main Findings:

Diagnostic accuracy

Test	Ref Test	Sample size	Sensitivity (%)	Specificity (%)	PPV (%)	NPV (%)
OIA (SHIGATOX)	Positives were confirmed by a Vero cytotoxicity assay Same as above	742 fresh stool samples	96.8/100^a	99.4/100^b	NR	NR
EIA (Premier EHEC)		742 fresh stool samples	83.9/96.8^a	99.8/100^b	NR	NR
OIA (SHIGATOX)	Positives were confirmed by a Vero cytotoxicity assay Same as above	85 frozen stool samples	88.5/88.0^a	100/100^b	NR	NR
EIA (Premier EHEC)		85 frozen stool samples	84.6/86.0^a	100/100^b	NR	NR

a: Sensitivity reported for direct stool samplel / broth enriched sample
b: Specificity reported for direct stool sample / broth enriched sample

Authors’ Conclusion:
“Overall, the OIA SHIGATOX kit provided rapid, easy-to-interpret results and was highly effective at detection of Shiga toxin-producing E. coli in fecal samples and overnight cultures.” P.3377

Vallieres,²
2013,
Canada

Main Findings:

Diagnostic accuracy

View in own window
Test Ref
Test Sample
size Sensitivity
(%) Specificity
(%) PPV
(%) NPV
(%)
EIA (Premier EHEC) rt-PCR 632 stool 28.6^a NR NR NR
EIA (ImmunoCard STAT!) rt-PCR 632 19.0^a NR NR NR
SMAC rt-PCR 632 23.8^a NR NR NR
a
Calculated from available data

Authors’ Conclusion:
“We conclude that PCR is specific and more sensitive than EIA. PCR should be considered for routine use in clinical settings where molecular detection facilities are available. Its lower limit of detection, equivalent to the infectious dose, is an obvious advantage for patient care and public health surveillance.” P.481

Wylie,²⁰
2013,
Canada

Main Findings:

Diagnostic accuracy

View in own window
Test Ref Test Sample
size Sensitivity
(%) Specificity
(%) PPV
(%) NPV
(%)
CHROMagar STEC Cytotoxin assay 205 85.7 95.8 60.0 98.9

Authors’ Conclusion:
“Although CHROMagar STEC is not recommended as a primary screen, our results indicate that it is an effective supplemental medium for the isolation of probable STEC. Given that current evidence suggests that there is an increasing prevalence of non-O157 STEC relative to O157:H7, coupled with the occurrence of several recent outbreaks associated with non-O157 STEC, the use of this medium in conjunction with other selective media will facilitate the isolation of many STEC serotypes.” P.470

Zhang,²¹
2012,
Germany

Main Findings:

Diagnostic accuracy

View in own window
Test Ref Test Sample
size Sensitivity
(%) Specificity
(%) PPV (%) NPV (%)
rt-M-PCR c-M-PCR + culture 132 stool samples (E,coli O104:H4) 100 100 NR NR

Authors’ Comment/Conclusion:
“A real-time multiplex PCR targeting stx2, wzyO104, and fliCH4 of enterohemorrhagic Escherichia coli (EHEC) O104:H4 correctly determined the presence or absence of these genes in 253 EHEC isolates and enrichment cultures of stool samples from 132 patients. It is a rapid, sensitive, and specific tool for detecting EHEC O104:H4 in human stools.”

: ASR = analyte specific reagent, c-PCR = conventional PCR, CT-SMAC = cefixime tellurite sorbitol MacConkey, EHEC = enterohemorrhagic E. coli, EIA = enzyme immunoassay, GPP = gastrointestinal pathogen panel, h = hour, HSLI = Hinton State Laboratory Institute, IMC = immunochromatography, m =- minute, MT-PCR = multiplex tandem PCR, NPA = negative percent agreement, NPV = negative predictive value, NR = not reported, OIA = optical immunoassay, PCR = polymerase chain reaction, PPA = positive percent agreement, PPV = positive predictive value, RPLA = reverse passive latex agglutination, rt-PCR = real time PCR, rt-M -PCR = real time multiplex PCR, SMAC = sorbitol MacConkey, std = standard, STEC = Shiga toxin producing E.coli

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Screening of Shiga-toxigenic Escherichia coli in Clinical Fecal Samples: A Review of Diagnostic Accuracy, Clinical Utility, Cost-Effectiveness and Guidelines [Internet]. Ottawa (ON): Canadian Agency for Drugs and Technologies in Health; 2015 Jul 8. APPENDIX 5, Main Study Findings and Authors’ Conclusions.
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