Table 1.
Characteristics of the included studies.
| Study ID | Country | Method | Sample size | Age (years)* | Emm type | Definition of invasive GAS |
| Bencardino et al., 2019 | Italy | PCR | Invasive (n = 5) Non-invasive (n = 116) |
NS | 1, 2, 4, 5, 6, 9, 11, 12, 18, 28, 29, 44, 48, 75, 78, 82, 87, 89, 118 | Isolates were from normally sterile fluids (blood and pleural fluid) |
| Bianco et al., 2006 | Italy | PCR | Invasive (n = 5) Non-invasive (n = 177) |
NS | None | A few strains were isolated from subjects affected by invasive diseases (bacteremia, pneumonia, and toxic shock-like syndrome) |
| Chan et al., 2009* | Hong Kong | PCR | Invasive (n = 27) Non-invasive (n = 27) |
53(4–100) | 1, 2, 3, 4, 9, 10, 11, 12, 22, 25, 28, 42, 49, 53, 54, 58, 63, 69, 70, 73, 75, 76, 77, 81, 82, 85, 86, 87, 88, 89, 90, 93, 94, 101, 104, 106, 112, 113, 118, 124, st9505, st2904, Stg485, STMRP6 | Invasive and non-invasive isolates were defined as recovery from sites that are usually sterile or non-sterile, respectively |
| Coppens et al., 2019 | Belgium | WGS | Invasive (n = 23) Non-invasive (n = 2) |
NS | 1 | Invasive GAS strains were randomly selected and obtained from blood and tissue [wounds/throat swabs obtained from patients with skin and soft-tissue infection (SSTI) body sites or were from an undefined origin] |
| Creti et al., 2005 | Italy | PCR | Invasive (n = 79) Non-invasive (n = 180) |
47.1 ± 23.6 | 1, 2, 3, 4, 5, 6, 9, 11, 12, 14, 18, 22, 27, 28, 29, 44, 50, 53, 59, 68, 75, 78, 80, 85, 87, 89, 102, 108, 110, 114, 118 | NS |
| Darenberg et al., 2007 | Sweden | Multiplex PCR | Invasive (n = 850) Non-invasive (n = 773) |
68(0–99) | 1, 4, 12, 28, 77, 89, 81 | Invasive disease was defined by isolation of GAS from blood samples or from samples obtained from other normally sterile sites |
| DelVecchio et al., 2002 | Australia | PCR | Invasive (n = 63) Non-invasive (n = 51) |
NS | None | Patients with invasive cases of disease (necrotizing fasciitis, toxic shock syndrome, cellulitis, bacteremia) |
| Descheemaeker et al., 2000 | Belgium | PCR | Invasive (n = 72) Non-invasive (n = 428) |
NS | 1, 3, 4, 6, 9, 11, 12 | GAS isolates from sterile sites (blood, sterile body fluids, abscesses, or tissue) of patients with invasive infections |
| Ekelund et al., 2005* | Denmark | PCR | Invasive (n = 200) Non-invasive (n = 352) |
(0.4–97.4) | 1, 2, 3, 4, 5, 6, 9, 11, 12, 22, 28, 29, 43, 49, 58, 70, 73, 75, 76, 77, 78, 87, 88, 89, 94, 102, 105, 109, 110, 27G, st1389, st3757 | Invasive GAS isolates obtained from normally sterile sites (blood, CSF, synovial fluid, pleural fluid, sterile aspirates, or tissue obtained during surgery or autopsy) |
| Golińska et al., 2016 | Poland | PCR | Invasive (n = 30) Non-invasive (n = 37) |
(18–50) | 1, 2, 3, 4, 12, 28, 75, 77, 89 | 12 S. pyogenes strains originated from tissues of women with puerperal fever, and 18 strains were isolated from blood of patients with sepsis |
| Haukness et al., 2002 | USA | PCR | Invasive (n = 17) Non-invasive (n = 63) |
NS | 1, 2, 3, 4, 5, 6, 12, 18, 22, 28, 59, 75, 77, 89 | Invasive GAS isolates cultured from normally sterile sites of pediatric patients |
| Hraoui et al., 2011 | Tunisia | Multiplex PCR | Invasive (n = 50) Non-invasive (n = 52) |
(2–93) | 1, 2, 3, 4, 6, 11, 12, 17, 18, 22, 26, 28, 33, 42, 43, 48, 59, 60, 63, 66, 67, 75, 76, 77, 81, 85, 87, 89, 92, 94, 102, 104, 106, 118, st1389, st2861UK, st3757, st432 | Invasive infection was defined as the isolation of GAS from sites that are usually sterile, including blood and cerebrospinal, peritoneal, pleural, and joint fluids, and deep tissue abscesses, or from a superficial site in association with STSS or NF |
| Hsueh, 1998 | Taiwan | PCR | Invasive (n = 44) Non-invasive (n = 28) |
(2–90) | 1, 6, 12 | Isolates from normally sterile sites were considered invasive |
| Jing et al., 2006 | China | PCR | Invasive (n = 10) Non-invasive (n = 76) |
NS | 1, 12, 8, 18, 80, 28, 101, 4, 66, 77, 94, 3, 6, 23, 44, 63, 64, 75, 85, 86, 88 | Invasive isolates were exclusively from blood |
| Khan et al., 2020 | Pakistan | PCR | Invasive (n = 41) Non-invasive (n = 33) |
NS | 1, 4, 28, 39, 42, 55, 58, 63, 65, 68, 75, 77, 88, 93, 104, 106 | S. pyogenes strains were procured isolated from various clinical specimens like pus, blood, wounds, tissues, body fluids, and synovial fluid |
| Kittang et al., 2011 | Norway | PCR | Invasive (n = 22) Non-invasive (n = 101) |
NS | 1, 3, 4, 12, 28, 82, 87, 89 | Invasive disease was defined by isolation of GAS, GCS, or GGS from a normally sterile site, or from a non-sterile site in combination with STSS or NF |
| Li et al., 2022 | USA | WGS | Invasive (n = 236) Non-invasive (n = 417) |
(0.4–99) | 1, 2, 3, 4, 6, 8, 9, 11, 12, 22, 28, 49, 59, 60, 68, 74, 75, 76, 77, 81, 82, 83, 87, 89, 92, 95, 118, 169 | An iGAS disease case was defined as illness with isolation of GAS from a normally sterile site or from a wound culture accompanied by necrotizing fasciitis or STSS in a resident of the surveillance area |
| Lintges et al., 2010 | Germany | Multiplex PCR | Invasive (n = 97) Non-invasive (n = 194) |
(0–88) | 1, 77, 28, 4, 12, 18, 75, 2, 3, 6, 49, 78, 22, 83, 95, 11, 81, 85, 94, 102, 44/61, 5, 9, 33, 58, 59, 7582, 89, 103, 108, 118, 29, 50, 66, 90, st3757, stns554, st1731 | Patients with invasive infections (blood samples and cerebrospinal fluid sample) |
| Luca-Harari et al., 2008 | Romania | Multiplex PCR | Invasive (n = 47) Non-invasive (n = 92) |
(0–83) | 1, 2, 3, 4, 5, 6, 8, 9, 12, 22, 23, 25, 28, 33, 44/61, 49, 50/62, 64, 65/69, 74, 75, 76, 77, 78, 81, 84, 87, 91, 92, 95, 100, 102, 106, 119 | Invasive cases were defined by the isolation of GAS from normally sterile sites (blood, CSF, pleurae, peritoneal or joint fluid, or deep tissue), or from a superficial site, in association with NF or STSS |
| Maripuu et al., 2008 | Sweden | PCR | Invasive (n = 54) Non-invasive (n = 37) |
NS | 1, 2, 3, 4, 6, 8, 12, 14, 19, 22, 28, 36, 41, 44, 49, 58, 66, 68, 73, 75, 81, 82, 84, 85, 89, 91, 93, 100 | The isolates were collected from patients with invasive infections: STSS, sepsis, and erysipelas |
| Meehan et al., 2018 | Ireland | PCR | Invasive (n = 442) Non-invasive (n = 492) |
43(15–69) | 1, 2, 3, 4, 5, 6, 9, 11, 12, 22, 28, 75, 76, 77, 81, 87, 89, 90 | iGAS cases were based on national case definitions |
| Michaelsen et al., 2011 | Norway | PCR | Invasive (n = 24) Non-invasive (n = 24) |
NS | 1, 3, 4, 6, 12, 18, 28, 77 | Invasive isolates consisting of NF and STSS |
| Muhtarova et al., 2017 | Bulgaria | Multiplex PCR | Invasive (n = 35) Non-invasive (n = 203) |
NS | None | Invasive isolates: punctures from peritonsillar abscesses, middle ears and sinuses, wounds, blood culture, and cerebrospinal fluid |
| Murakami et al., 2002 | Japan | PCR | Invasive (n = 17) Non-invasive (n = 299) |
NS | 1, 2, 3, 4, 6, 11, 12, 13, 18, 28, 58, 75, 87, 89 | Invasive isolates were obtained from blood or an unknown location |
| Mylvaganam et al., 2000 | Norway | PCR | Invasive (n = 22) Non-invasive (n = 20) |
NS | 1, 3, 6, 22, 28, 75, 78 | Invasive isolates were from necrotizing fasciitis, streptococcal toxic shock syndrome, and septicemic patients without necrotizing fasciitis |
| Nandi et al., 2002 | India | PCR | Invasive (n = 8) Non-invasive (n = 52) |
(5–15) | None | NS |
| Plainvert et al., 2014 | France | PCR | Invasive (n = 435) Non-invasive (n = 138) |
(0–97) | 1, 2, 3, 4, 5, 6, 8, 9, 11, 12, 18, 22, 24, 25, 27, 28, 29, 30, 32, 33, 41, 42, 43, 44, 48, 49, 50, 53, 55, 58, 59, 60, 63, 64, 65, 66, 68, 69, 71, 73, 74, 75, 76, 77, 78, 81, 82, 83, 85, 87, 88, 89, 90, 92, 93, 94, 100, 101, 102, 103, 104, 106, 108, 110, 112, 113, 116, 117, 118, 122, 124, 142, 147, 158, 168, 172, 174, 176, 179, 180, 182, 183, 187, 192, 217, 230, stG1750 | GAS invasive infection was defined as the isolation of bacteria from a usually sterile site (e.g., blood, cerebrospinal fluid, bone, or joint fluid) or from samples obtained from a non-sterile site in combination with the clinical signs of NF or STSS |
| Rivera et al., 2006 | Spain | PCR | Invasive (n = 27) Non-invasive (n = 99) |
(0–91) | 1, 2, 3, 4, 6, 9, 11, 12, 18, 22, 25, 28, 29, 43, 44, 49, 50, 58, 59, 63, 64, 70, 75, 77, 81, 83, 87, 89, st11014 | Invasive infection was defined as the recovery of GAS from sites that are usually sterile, including blood and cerebrospinal, peritoneal, pleural, and joint fluids; deep tissue abscesses; and a superficial site in clinical association with STSS or NF |
| Schmitz et al., 2003 * | 12 European countries | PCR | Invasive (n = 153) Non-invasive (n = 25) |
NS | 1, 3, 12, 28 | Among the 202 SENTRY isolates, 149 were blood-culture isolates, 31 were wound isolates, and 22 were pharynx isolates |
| Strus et al., 2017 | Poland and Germany | PCR | Invasive (n = 48) Non-invasive (n = 205) |
NS | 1, 2, 3, 4, 6, 11, 12, 27G, 28, 32, 44, 58, 66, 73, 75, 77, 78, 81, 89, 108, 122, 159, 123 | Strains were isolated from wounds and deep skin infections |
| Tyler et al., 1992 | Canada | PCR | Invasive (n = 21) Non-invasive (n = 114) |
NS | None | NS |
| Yu et al., 2021 | China | PCR | Invasive (n = 32) Non-invasive (n = 310) |
<18 | 1, 2, 3.1, 4, 6, 12, 22, 28, 75 | The strains were isolated from blood |
*Ekelund et al. reported on 200 iGAS out of 201.
*Schmitz et al. reported on 153 iGAS out of 239 and 25 non-iGAS out of 53.
NS, not stated. *Chan et al. used a random subset of the original 285 GAS isolates. **Age reported as per the publication. Brackets denote min–max range.
*Luca-Harari et al. reported on 47 iGAS and 92 non-iGAS, as seen in Table 2 of the article.
*Meehan et al. reported on 442 iGAS out of 473 and 492 non-iGAS out of 517.