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Correction: Review: a comprehensive summary of a decade development of the recombinase polymerase amplification

Jia Lia, Joanne Macdonald*bc and Felix von Stetten*ad
aLaboratory for MEMS Applications, IMTEK – Department of Microsystems Engineering, University of Freiburg, Georges-Köhler-Allee 103, 79110 Freiburg, Germany. E-mail: Felix.von.Stetten@Hahn-Schickard.de; Tel: +49 761 203-73243
bInflammation and Healing Research Cluster, Genecology Research Centre, School of Science and Engineering, University of the Sunshine Coast, Qld, Australia. E-mail: jmacdon1@usc.edu.au; Tel: +61 7 5456 5944
cDivision of Experimental Therapeutics, Columbia University, New York, NY, USA. E-mail: jm2236@columbia.edu
dHahn-Schickard, Georges-Köhler-Allee 103, 79110 Freiburg, Germany

Received 19th December 2019 , Accepted 19th December 2019

First published on 23rd January 2020


Correction for ‘Review: a comprehensive summary of a decade development of the recombinase polymerase amplification’ by Jia Li et al., Analyst, 2019, 144, 31–67.


The authors regret that the original version of the review contained some incorrect data. Corrections to the original article are listed as follows.

Some of the values in Table 5 were incorrect. The corrected version of Table 5 is presented below.

Table 5 RPA literature describing clinical/field trials
Analyte(s) Detection method Limit of detection Clinical/field sample(s) Clinical sensitivity Clinical specificity Benchmark method Limit of detection of benchmark method Clinical sensitivity of benchmark method compared to RPA Clinical specificity of benchmark method compared to RPA Ref.
a RT: reverse transcription.b Clinical sensitivity and specificity were recalculated using the ESI.
Nucleocapsid (N) gene of bovine coronavirus Real-time fluorescent detection 10 to 100 RNA copies (19 RNA copies by probit analysis) 16 fecal and 14 nasal swab specimens collected from cattle showing intestinal and/or respiratory manifestations 100% 100% Real-time RTa-PCR 1000 RNA copies The same The same 125
Chlamydia trachomatis CDS2 gene Lateral flow strip detection 5–12 pathogens/reaction 70 self-collected first void morning urine samples from young adults (19 males and 51 females) 83% 100% Roche Cobas Amplicor CT assay Higher The same 92
cAMP factor (cfb) gene of group B streptococci Real-time fluorescent detection 98 genome copies 50 vaginal/anal samples collected from women 96% 100% Real-time PCR Higher The same 126
DNA target sequence specific to Cryptosporidium spp. Lateral flow strip detection 100 oocysts per mL stool A total of 10 human stool samples clinically verified to contain cryptosporidium by a reference laboratory and 11 stool samples from healthy volunteers presumed to be uninfected 100% 100% Real-time PCR Lower The same 127
5′-Untranslated region of Yellow fever virus (YFV) Real-time fluorescent detection on the tube scanner 44 genomic copies/reaction in YFV RNA extracts; 21 genomic copies/reaction of YFV-spiked human plasma samples 34 samples of monospecific pools of wild-caught mosquitoes collected from Kedougou, southern Senegal 80% 100% Real-time RTa-PCR 8 genomic copies/reaction in YFV RNA extracts Higher The same 117
Real-time fluorescent detection on the microfluidic platform 27 RNA samples of mosquito pools 71.4% 100% Higher The same
IS6110 gene of Mycobacterium tuberculoss (MTB) Real-time fluorescent detection 6.25 fg 121 specimens including induced and expectorated sputum (n = 119) and respiratory washes (bronchial and tracheal, n = 2) collected from a total of 101 tuberculosis suspect cases (no more than 3 specimens/individual were tested) 87.5% 95.4% Culture Higher Higher 128
IS1081 gene of Mycobacterium tuberculoss 20 fg 91.4% 100% Higher The same
Giardia beta giardin gene Lateral flow strip detection 103–103.5 cysts per mL of stool 104 clinical stool samples 73% 96% Real-time PCR 102.5 cysts per mL of stool Higher Higher 129
IS6110 gene of Mycobacterium tuberculoss Real-time photonic detection 10−6-Fold diluted MTB sample 42 clinical samples including 13 smear and culture positive samples and 22 smear and culture negative samples 86% 95% Real-time PCR Higher Higher 130b
A highly conserved 3′-untranslated region that cover DENV 1–4 Real-time fluorescent detection DENV serotype 1: 237 RNA copies; DENV serotype 2: 618 RNA copies; DENV serotype 3: 363 RNA copies; DENV serotype 4: 383 RNA copies Inactivated DENV 1–4 spiked plasma and 31 DENV positive samples in Kedougou region in Senegal 98% Real-time RTa-PCR Higher 131
RNA of 90 plasma samples extracted and tested between 2012–2013 by RTa-PCR in Bangkok (Thailand) 72% Higher
47 kDa gene sequence from the Karp strain of Orientia tsutsugamushi (47-RPA) and the 17 kDa gene sequence from the Wilmington strain of Rickettsia typhi Lateral flow strip detection 47 kDa gene: 53 DNA copies/reaction 10 positive and 10 negative human samples 80% 100% Real-time PCR 47 kDa gene: 10 DNA copies/reaction Higher Higher 95
17 kDa gene: 20 copies/reaction 17 kDa gene: 6 DNA copies/reaction
Ribosomal 18S DNA of Entamoeba histolytica Lateral flow strip detection 2.5 fg from serial dilutions of pure DNA extracted from parasites; 40 parasites from spiked stool sample 32 samples of DNA extracted from clinical samples 100% 100% Real-time PCR 2.5 fg from serial dilutions of pure DNA extracted from parasites The same The same 132
A sequence designed based on ITS sequences of the Madurella mycetomatis type strain CBS 109801 Gel electrophoresis detection 0.23 ng of DNA 12 patient biopsy specimens 100% 100% Conventional PCR The same The same 133
Ebola virus (EBOV) nucleocapsid sequence Real-time fluorescent detection 5 genomic copies/reaction of a molecular RNA standard; 15 genomic copies/reaction in EBOV-spiked human plasma samples 928 post-mortem swab samples 100% 100% Real-time RTa-PCR The same The same 134
Orf virus (ORFV) DNA polymerase gene segments Real-time fluorescent detection 100 DNA copies 22 samples collected from suspected cases of Orf, 8 nasal swabs collected from experimentally infected sheep and 5 samples obtained from healthy goats 86% 100% Real-time PCR Higher The same 135
Leader peptidase A (LepA) gene of Streptococcus pneumoniae Real-time fluorescent detection 4.1 genome equivalents/reaction 15 blood samples including 11 confirmed culture positive and 4 confirmed culture negative for Streptococcus pneumoniae 100% 100% Real-time PCR 5.1 genome equivalents/reaction The same The same 97
Orf virus (ORFV) DNA polymerase gene segments Lateral flow strip detection 80 copies/reaction of DNA plasmid 24 ORFV-spiked tissues samples, 53 samples collected from goats with suspected ORFV infection, 8 nasal swabs samples and 5 tissues samples from healthy goats 100% 100% Real-time PCR The same The same 64
Leishmania donovani (LD) kinetoplast minicircle DNA Real-time fluorescent detection 100 DNA copies applying the LD DNA linearised plasmid; 1 genomic DNA copy 96 buffy coats and skin biopsies collected from visceral leishmaniasis, asymptomatic and post-kala-azar dermal leishmaniasis 100% 100% Real-time PCR The same The same 121
Highly pathogenic porcine reproductive and respiratory syndrome virus (HP-PRRSV) NSP2 gene Real-time fluorescent detection 70 RNA copies/reaction 68 tissue samples and 10 serum samples collected from suspected pigs of HP-PRRSV, 35 serum samples and 12 tissue samples collected from healthy pigs 97.6% 100% Real-time RTa-PCR Higher The same 136
100% conserved sequence of a major capsid protein gene of all cyprinid herpesvirus 3 strains Gel electrophoresis detection 10 copies of genomic DNA 12 confirmed latently infected fish and 1 confirmed uninfected fish 100% 100% Real-time PCR Lower The same 66
cAMP factor (cfb) gene of group B streptococci Real-time fluorescent detection 6.25–12.5 genome equivalents 124 clinical samples 100% 100% Real-time PCR 3.1–6.25 genome equivalents The same The same 137
Non-structure protein 1 (nsP1) of Chikungunya virus (CHIKV) Real-time fluorescent detection 80 genome copies of extracted RNA from CHIKV isolate LR strain 58 suspect Chikungunya fever cases 100% 100% Real-time RTa PCR 80 genome copies of extracted RNA from CHIKV isolate LR strain The same The same 87
A sequence designed in NS2A region conserved among all Zika virus lineages Real-time fluorescent detection 21 RNA copies 25 positive and 9 negative urine samples collected during the Zika virus epidemic in Tuparetama, Brazil 92% 100% Real-time RTa-PCR Higher The same 138
G-protein-coupled chemokine receptor (GPCR) gene of lumpy skin disease virus (LSDV) Real-time fluorescent detection 100 DNA copies (179 DNA copies by probit analysis) 12 negative skin samples and 22 skin nodules of suspected LSDV-infected cattle collected during the summer of 2012 in Dakahlia Governorate, Egypt 100% 100% Real-time PCR 37 DNA copies The same The same 139
IS900 gene of Mycobacterium avium subsp. paratuberculosis (MAP) Real-time fluorescent detection 16 plasmid copies per μL; 500 fg genomic DNA/reaction Archived DNA of MAP positive blood (n = 14), sperm (n = 18), faecal (n = 12) and tissue (n = 4) samples and 20 MAP-negative faecal samples 89.5% Real-time PCR 1 plasmid copies per μL; 50 fg genomic DNA/reaction Higher 140
T1E4 gene of prostate cancer Real-time fluorescent detection 1000 RNA copies 9 urine samples obtained from prostate cancer and 2 urine samples from healthy individuals 90% 100% Real-time RTa-PCR The same The same 141
NS1 gene of porcine parvovirus (PPV) Real-time fluorescent detection 300 DNA copies 101 clinical tissue samples (serum, liver, kidney, lymph node, spleen and duodenum) collected from pig farms with suspected cases of PPV in Gansu province, China, and 27 clinical samples (serum, kidney and duodenum) collected from healthy pigs 94.4% 100% Real-time PCR Higher The same 54
Nucleocapsid gene of type 2 porcine reproductive and respiratory syndrome virua (PRRSV) Real-time fluorescent detection 100 RNA copies (690 RNA copies by probit analysis) 60 clinical samples (lymph node, lung, spleen and liver) collected from diseased pigs suspected of having PRRS from 5 pigs farms in Hebei province, China from 2015–2016 Real-time RTa-PCR 100 RNA copies 142
Cytochrome b gene of Theileria annulata Lateral flow strip detection 2 pg genomic DNA 17 anticoagulated blood samples collected from tropical theileriosis endemic areas in Gansu province, China Real-time PCR 67
pirA-like gene of Vibrio owensii Real-time fluorescent detection 2 plasmid copies (2.84 plasmid copies by probit analysis) 138 clinical shrimp obtained from immersion bioassay, including 70 shrimp acute hepatopancreatic necrosis disease (AHPND) infected shrimp and 68 non-AHPND infected shrimp 100% 100% Real-time PCR Lower Lower 143
rRNA gene of Fasciola hepatica Gel electrophoresis detection 1.6 pg μL−1 DNA copies 102 human stool samples selected from banked specimens 87.8% 100% Real-time PCR 1.6 pg μL−1 DNA copies Lower The same 144
Lateral flow strip detection 1.0 pg μL−1 DNA copies 95.2% 90.4% Lower Higher
N gene of pest des petits ruminants virus (PPRV) Real-time fluorescent detection 100 plasmid copies 32 clinical samples collected from suspected cases of PPRV in Gansu province, China and 5 samples obtained from healthy sheep 90% 100% Real-time RTa-PCR 10 plasmid copies Higher The same 145
Lateral flow strip detection 150 plasmid copies 90% 100% Higher The same
ITS2 gene of Phytophthora infestans Real-time fluorescent detection 50 fg μL−1 of genomic DNA 24 potato leaf samples collected from fields with and without visible symptoms of late blight infections in New Brunswick and Quebec provinces, Canada, respectively 33.3% 100% LAMP 50 fg μL−1 of genomic DNA Higher Lower 146
ORF2 gene of porcine circovirus type 2 (PCV2) Real-time fluorescent detection 100 plasmid copies 65 clinical samples (spleen, inguinal lymph node, tonsil, lung and serum) collected from suspected PCV2 infection pigs from 8 pig farms in Shandong province, China; 37 clinical samples (inguinal lymph node, tonsil, lung and serum) collected from Gansu Province, China, and 10 PCV1 positive samples conserved in the laboratory 100% 100% Real-time PCR 80 plasmid copies The same The same 69
Lateral flow strip detection 100 plasmid copies 100% 100% The same The same
gD gene of pseudorabies virus Real-time fluorescent detection 100 DNA copies 76 clinical samples (tonsil, heart, spleen, lymph nodes, lung and serum) collected from pig farms in Shandong province, China, and 26 clinical samples (lymph nodes, tonsil and serum) collected from healthy pigs 93.3% 100% Real-time PCR Higher The same 70
Lateral flow strip detection 160 DNA copies 93.3% 100% Higher The same
B1 gene of Toxoplasma gondii Lateral flow strip detection 0.1 oocysts/reaction 35 soil samples and 15 water samples collected from parks, residential areas, schools and gutterways in Lanzhou city, Gansu rovince, China, during August 2016 100% 100% Nested PCR 1 oocyst/reaction The same The same 71
RNA transcript of TMPRSS2:ERG (a fusion gene for prostate cancer) RPA fluocculation assay 105 RNA copies Clinical urine specimens from 10 metastatic castration-resistant promising prostate cancer patients and 5 healthy control patients 70% 100% Conventional RTa-PCR The same The same 101
VP2 gene of porcine parvovirus Real-time fluorescent detection 100 DNA copies (103 DNA copies by probit analysis) 115 clinical samples (lymph node, lung, spleen, kidney and duodenum collected from pigs with reproductive disorders, diarrhea or respiratory disease in Hebei province, China from 2014 to 2016 100% 100% Real-time PCR 100 DNA copies The same The same 147
G-protein-coupled chemokine receptor (GPCR) gene of Capripoxvirus Real-time fluorescent detection 300 plasmid copies 107 clinical samples (liver, lung, kidney, spleen, skin and blood) collected from 14 suspected sheep and 6 suspected goats in Gansu province which were characterised by pyrexia, excessive salivation and generalised pock lesions in the skin during the period of October 2014 to August 2015 97% 100% Real-time PCR Higher The same 148
Lateral flow strip detection 300 plasmid copies 97% 100% Higher The same
Nucleocapsid protein gene of canine distemper virus Real-time fluorescent detection 9.4 RNA copies (31.8 RNA copies by probit analysis) 32 nasal/oropharyngeal swabs collected from 20 dogs of both sexes (various breeds and ages) from the animal hospital of Agricultural University of Hebei and 12 raccoon dogs from the farms in Hebei Province, China from 2014 to 2016 100% 100% Real-time RTa-PCR 94 RNA copies The same The same 149
imp gene of Candidatus Phytoplasma oryzae Real-time fluorescent detection 1–10 plasmid copies 66 Napier grass samples from various geographical locations in western Kenya 100% 57.1% Real-time PCR Lower The same 79
Lateral flow strip detection 10–100 plasmid copies
imp gene of Candidatus Phytoplasma mali Real-time fluorescent detection 10 copies of cloned plasmid 38 roots of field samples from apple (Malus domestica) trees collected in autumn 2014, in spring 2015 and in June 2016 in private orchards or in the experimental field of the Institute for fruit growing in Samochvalovichi, Belarus 100% 100% Real-time PCR The same The same 72
Lateral flow strip detection 10 copies of cloned plasmid 100% 100% The same The same
N gene of rabies Real-time fluorescent detection 1000 RNA copies per μL of strains SAD B19, Bobcat USA and Kelev A panel of RNA from 33 field samples 97% Real-time PCR 1 RNA copies per μL of strains SAD B19, Bobcat USA and Kelev Higher 150
KRAS oncogenic mutation gene G12D on Exon 12 Real-time silicon photonic microring-based detection 1% to 100% of the mutant cells 70 frozen tissues samples from colorectal cancer patients in Bio-Resource Center of Asian Medical Center, including 24 samples with the G12D mutation (34.3%), 26 samples with G13D mutation (37.1%) and 20 samples with no mutation (28.6%) 100% 100% Conventional PCR 30% to 100% of the mutant cells Lower The same 151
KRAS oncogenic mutation genes G13D on Exon 13 100% 100% Lower The same
A consensus region that covers all 7 S-segment clades of Crimean-Congo Hemorrhagic fever virus (CCHFV) Real-time fluorescent detection 500 RNA copies (251 RNA copies by probit analysis) 21 extracted patient sera samples obtained in relation to outbreaks of CCHFV in 2013–2015 in Tajikistan 88% 100% Real-time PCR Higher The same 152
Canine parvovirus 2 (CPV-2) nucleocapsid protein gene Real-time fluorescent detection 10 copies of recombinant plasmid 91 fecal swab samples collected from the dogs from 2012 to 2016 100% 100% Real-time PCR 10 copies of recombinant plasmid The same The same 153
G gene of bovine ephemeral fever virus (BEFV) Lateral flow strip detection 8 plasmid copies/reaction (corresponding to 24 RNA copies) 104 clinical blood specimens and 24 tissue samples including 16 lung tissue specimens, 8 lymph gland specimens collected from suspected dairy cattle cases of BEFV infections in eastern China 97.89% 90.91% Real-time PCR Higher Higher 74
IS900 gene of Mycobacterium avium subsp. paratuberculosis Lateral flow strip detection 8 plasmid copies/reaction 320 individual fecal samples collected between September 2016 and September 2017 from 10 different dairy farms located in 10 distinct geographic regions of Shandong province, China 100% 97.63% Real-time PCR 8 plasmid copies/reaction The same Higher 77
Fno FSC771 hypothetical protein gene of Francisella noatunensis subsp. Orientalis Real-time fluorescent detection 10 plasmid copies (15 plasmid copies by probit analysis) Samples of spleen (n = 78), head kidney (n = 78) and water (n = 5) 100% 84.89% Real-time PCR 10 plasmid copies (11 plasmid copies by probit analysis) The same Higher 154
VP1 gene of Enterovirus 71 subgenotype C4 (EV71-C4) Real-time fluorescent detection 3.767[thin space (1/6-em)]log[thin space (1/6-em)]10 genomic copies (LGC) Stool samples (n = 44) collected in 2017 by Shenzhen Center for Disease Control and Prevention 100% 100% Real-time PCR 2.026[thin space (1/6-em)]log[thin space (1/6-em)]10 genomic copies (LGC) The same The same 155
Stool samples (n = 134) collected from patients with suspected hand–foot–mouth disease at the pediatrics department of Zhujiang Hospital (Southern Medical University, Guangzhou, China) in 2009 89.5% 100% Lower The same
56 kDa gene of a Karp-like strain of Orientia tsutsugamushi Lateral flow strip detection 10 copies (recombinant plasmid); 12 copies of genomic DNA 62 animal (including Apodemus agrarius, Rattus norvegicus, Microtus fortis and Neomys fodiens) organ samples including 5 infected animals trapped in the wild, 2 infected in the laboratory and 55 uninfected animals trapped in the wild 100% 100% Real-time PCR 12 copies of genomic DNA The same The same 156
23S rRNA gene of Coxiella burnetii Lateral flow strip detection 10 copies (recombinant plasmid); 7 copies of genomic DNA DNA of spleens from 5-week old C57BL/6 female Coxiella burnetii-infected mice and 9 control PBS-infected mice 100% 100% Real-time PCR 7 copies of genomic DNA The same The same 157


In section 2.3, data from ref. 41 were not cited correctly and should be removed. The respective passage should read as follows: “However, shorter amplicons (79 nucleotides;37 94 nucleotides38–40) and longer amplicons up to 1500 nucleotides6 have also been reported.”

In the Fig. 2 caption, “(Bsu or Sau)” should be removed after “recombinase” and inserted after “polymerase”. The corrected passage should read as follows: “The recombinase disassembles from the nucleoprotein filament once the strand exchange is performed, and will be available for the next pair of primers. Next, the DNA polymerase (Bsu or Sau) extends from the 3′ end of primers.”

In section 2.5, ref. 76 is not relevant as it is the same as ref. 77, and should be disregarded. The respective passage should read as follows: “However, several research groups have studied RPA reaction temperatures that lie outside of the recommended range.38,44,45,60,62–75,77,78 The largest temperature range was tested between 15 °C and 50 °C;62,64,69,70,77 and results indicated the marginal reaction temperature to produce a positive result should be greater than 30 °C.62–64,66,67,69,71,74,77

In section 2.5, ref. 63 was not interpreted correctly. The corrected text should read: “Moreover, Lillis et al.63 showed that the ambient temperature also had an effect on RPA reaction: the RPA reaction was unstable if the ambient temperature was below 30 °C, even at extended reaction time.”

In section 2.8, ref. 107 is not required and should be deleted. The corrected passage should read: “For the TwistAmp® nfo kit, however, two types of amplicons are generated… (note that only the dual-labelled product will generate a positive signal in the test zone of a lateral flow strip detection based on a sandwich assay).105,106,108

In section 2.8, the problems reported in ref. 117 were not sufficiently reflected in the original version of the review. Ref. 117 should be reported separately and the passage should read as follows: “As with lateral flow strip detection, direct usage of RPA amplicons is possible, but it is recommended to dilute the amplicons with the running buffer (e.g. 1/100 dilution) before running on the strip to (1) improve its wicking performance114 and (2) avoid “faint ghost band” effects.45,54,115,116 However, the dilution of the amplicon does not always prevent the appearance of a faint band, which can lead to specificity problems in the assay.117

In section 3.2, ref. 166 was not cited correctly. The corrected version should read: “Results suggest that electrochemical detection could be up to 10-fold more sensitive than optical detection (by enzyme linked oligonucleotide assay).166

In section 3.2, a reference was not provided for the sensitivity of the GeneXpert MTB/RIF assay. A reference should be added to the end of the following passage: “This ruthenium compound-based electrochemical detection achieved 11 CFU mL−1 of Mycobacterium tuberculosis analytical sensitivity, which is even more sensitive than the GeneXpert MTB/RIF (Cepheid Inc.) detection (a World Health Organisation recommended tuberculosis diagnostic system that employs PCR real-time fluorescent detection; 131 CFU mL−1).” The added reference is shown below as ref. 1.

In section 3.4, ref. 113 was not cited correctly. Instead of Mycobacterium bovis, Mycobacterium tuberculosis was used for demonstration. The corrected sentence should read: “Liu et al.113 demonstrated a duplex detection of IS6110 and IS1081 insertion sequences of Mycobacterium tuberculosis using RPA-SMR assay, and achieved 3.2 and 12 genomic DNA copies per reaction analytical sensitivity respectively.”

In section 4.1, ref. 182 and 183 were not cited precisely. The corrected version of the text should read: “The “microcliff” structured microchip demonstrated by Yeh et al. encased 200 to 1500 wells (30–100 nL per well),182 and 224 wells (100 nL per well),183 which allowed detection of 103–105 and 10–105 copies per μL of MRSA DNA, respectively.”

In section 4.2, ref. 194 should be deleted after the following sentence: “For the latter, one demonstration is on the digital video disk (DVD) by Maquieira research group, and the resulting signals can be detected by a DVD player (Fig. 12B).188,191

Ref. 101 in the original article was incorrect and should be replaced with the correct reference, shown below as ref. 2.

Ref. 107 was not cited in the original article and should be disregarded.

The Royal Society of Chemistry apologises for these errors and any consequent inconvenience to authors and readers.

Acknowledgements

The authors thank Valentina Paz Gacitúa Miranda, Hahn-Schickard, for thoroughly studying all of the referenced literature and for spotting gaps and mistakes.

References

  1. World Health Organization, Xpert MTB/RIF Implementation Manual: Technical and Operational ‘How-To’; Practical Considerations. No. WHO/HTM/TB/2014.1. World Health Organization, 2014, Geneva, Switzerland, ISBN: 978 92 4 150670 0.
  2. K. M. Koo, E. J. Wee, P. N. Mainwaring and M. Trau, Sci. Rep., 2016, 6, 30722 CrossRef CAS PubMed.

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