Ecology and Genetic Lineages of Nasal Staphylococcus aureus and MRSA Carriage in Healthy Persons with or without Animal-Related Occupational Risks of Colonization: A Review of Global Reports

Abstract

In this conceptual review, we thoroughly searched for appropriate English articles on nasal staphylococci carriage among healthy people with no reported risk of colonization (Group A), food handlers (Group B), veterinarians (Group C), and livestock farmers (Group D) published between 2000 and 2021. Random-effects analyses of proportions were performed to determine the pooled prevalence of S. aureus, MRSA, MRSA-CC398, and MSSA-CC398, as well as the prevalence of PVL-positive S. aureus from all eligible studies. A total of 166 eligible papers were evaluated for Groups A/B/C/D (n = 58/31/26/51). The pooled prevalence of S. aureus and MRSA in healthy humans of Groups A to D were 15.9, 7.8, 34.9, and 27.1%, and 0.8, 0.9, 8.6, and 13.5%, respectively. The pooled prevalence of MRSA-CC398 nasal carriage among healthy humans was as follows: Group A/B (<0.05%), Group C (1.4%), Group D (5.4%); and the following among Group D: pig farmers (8.4%) and dairy farmers (4.7%). The pooled prevalence of CC398 lineage among the MSSA and MRSA isolates from studies of the four groups were Group A (2.9 and 6.9%), B (1.5 and 0.0%), C (47.6% in MRSA), and D (11.5 and 58.8%). Moreover, MSSA-CC398 isolates of Groups A and B were mostly of spa-t571 (animal-independent clade), while those of Groups C and D were spa-t011 and t034. The MRSA-CC398 was predominately of t011 and t034 in all the groups (with few other spa-types, livestock-associated clades). The pooled prevalence of MSSA and MRSA isolates carrying the PVL encoding genes were 11.5 and 9.6% (ranges: 0.0-76.9 and 0.0-28.6%), respectively. Moreover, one PVL-positive MSSA-t011-CC398 isolate was detected in Group A. Contact with livestock and veterinary practice seems to increase the risk of carrying MRSA-CC398, but not in food handlers. Thus, this emphasizes the need for integrated molecular epidemiology of zoonotic staphylococci.

Keywords: CC398; CoNS; MRSA; S. pseudintermedius; Staphylococcus aureus; genetic lineages; livestock; nasal colonization.

Figure 1

Identification and selection flowchart of articles on nasal staphylococci carriage in healthy human.

Figure 2

Pooled prevalence of S. aureus nasal carriage among healthy people with or without occupational risks of colonization (Groups A–D) by continent (a) and grouped by countries (b): (i) Africa; (ii) Asia; (iii) Europe; (iv) America and Australia. The number of studies per continent in Groups A, B, C, and D, respectively, were as follows: Africa (13, 10, 2, and 7); Asia (16, 11, 2, 5); Europe (22, 7, 2, and 9); America and Australia (12, 3, 1, and 5).

Figure 2

Pooled prevalence of S. aureus nasal carriage among healthy people with or without occupational risks of colonization (Groups A–D) by continent (a) and grouped by countries (b): (i) Africa; (ii) Asia; (iii) Europe; (iv) America and Australia. The number of studies per continent in Groups A, B, C, and D, respectively, were as follows: Africa (13, 10, 2, and 7); Asia (16, 11, 2, 5); Europe (22, 7, 2, and 9); America and Australia (12, 3, 1, and 5).

Figure 3

Percentage of eligible studies carried out on healthy humans of Groups A–D showing different rates of MRSA nasal carriage. NB—The number of eligible studies on nasal MRSA carriage per Groups A, B, C, and D were 52, 21, 25, and 49, respectively (included in Table 2).

Figure 4

Pooled prevalence of MRSA nasal carriage among healthy people with or without occupational risks of colonization (Groups A-D) by continent (a) and grouped by countries/continents (b). In each country, the indicated pooled prevalence in each group (A–D) was analyzed in an independent way. The number of studies per continent in Groups A, B, C, and D, respectively, were as follows: Africa (10, 5, 3, and 8); Asia (17, 9, 4, 11); Europe (12, 6, 13, and 24); America and Australia (13, 1, 5, and 6).

Figure 4

Pooled prevalence of MRSA nasal carriage among healthy people with or without occupational risks of colonization (Groups A-D) by continent (a) and grouped by countries/continents (b). In each country, the indicated pooled prevalence in each group (A–D) was analyzed in an independent way. The number of studies per continent in Groups A, B, C, and D, respectively, were as follows: Africa (10, 5, 3, and 8); Asia (17, 9, 4, 11); Europe (12, 6, 13, and 24); America and Australia (13, 1, 5, and 6).

Figure 5

Pooled rates of MRSA, MRSA-CC398, and MSSA-CC398 nasal carriage in the healthy individuals of the Groups A–D, and rate of CC398 lineage in relation to MRSA and MSSA isolates. NB-a—Pooled MRSA rates were obtained from the Supplementary Tables S1–S4 and pooled MRSA-CC398 and MSSA-CC398 data of Table S7; b—No study reported MRSA-CC398 lineage in food handlers; c—None of analyzed studies carried out molecular typing of nasal MSSA in Group C; d—There were only two studies (of 13 eligible) that identified MRSA-CC398 in healthy people without risk of nasal colonization; e—There were two studies (of 5 eligible) that reported MSSA-CC398 in food handlers.

Figure 6

Pooled rates of MRSA, MRSA-CC398, and MRSA-CC398/ST9 nasal carriage in livestock farmers (group D). NB-a—Pooled MRSA rates in farmers were obtained from Supplementary Table S4 and pooled MRSA-CC398 and MSSA-CC398 from Supplementary Table S7; b—There were 19 and 5 studies in which we performed molecular typing of MRSA in pig and dairy farmers, respectively; c—There were 4 molecular typing studies classified as others (chicken and unspecified/mixed type of farmers).

Figure 7

Pooled rates of MRSA, MRSA-CC398, and MRSA-CC398/ST9 nasal carriage in pig farmers depending on the continent of origin, and rate of CC398 lineage in relation to MRSA isolates. NB—Only one study from Australia on 52 pig farmers was included in this analysis.

Figure 8

Geographic distribution of CC398 isolates detected in healthy humans of groups A, C, and D (spa types identified). (a) Group A (green) and C (blue); (b) Group D (purple). No CC398-MRSA was reported in Group B. Citations for Figure 8a: China [49], Austria [62], Belgium [62], Croatia [62], Netherlands [62], Germany [62], Switzerland [121,122,123], Denmark [124], Czech Republic [135], UK [136]. Citations for Figure 8b: Poland [125], Korea [152], China [155], Switzerland [121,168], Italy [161,167], Germany [172,174,175], Spain [181], Netherlands [181], USA [184], Canada [186].

Figure 8

Geographic distribution of CC398 isolates detected in healthy humans of groups A, C, and D (spa types identified). (a) Group A (green) and C (blue); (b) Group D (purple). No CC398-MRSA was reported in Group B. Citations for Figure 8a: China [49], Austria [62], Belgium [62], Croatia [62], Netherlands [62], Germany [62], Switzerland [121,122,123], Denmark [124], Czech Republic [135], UK [136]. Citations for Figure 8b: Poland [125], Korea [152], China [155], Switzerland [121,168], Italy [161,167], Germany [172,174,175], Spain [181], Netherlands [181], USA [184], Canada [186].