A Sequalae of Lineage Divergence in Staphylococcus aureus from Community-Acquired Patterns in Youth to Hospital-Associated Profiles in Seniors Implied Age-Specific Host-Selection from a Common Ancestor

Abstract

The rapidly changing epidemiology of Staphylococcus aureus and evolution of strains with enhanced virulence is a significant issue in global healthcare. Hospital-associated methicillin-resistant S. aureus (HA-MRSA) lineages are being completely replaced by community-associated S. aureus (CA-MRSA) in many regions. Surveillance programs tracing the reservoirs and sources of infections are needed. Using molecular diagnostics, antibiograms, and patient demographics, we have examined the distributions of S. aureus in Ha'il hospitals. Out of 274 S. aureus isolates recovered from clinical specimens, 181 (66%, n = 181) were MRSA, some with HA-MRSA patterns across 26 antimicrobials with almost full resistances to all beta-lactams, while the majority were highly susceptible to all non-beta-lactams, indicating the CA-MRSA type. The rest of isolates (34%, n = 93) were methicillin-susceptible, penicillin-resistant MSSA lineages (90%). The MRSA in men was over 56% among total MRSA (n = 181) isolates and 37% of overall isolates (n = 102 of 274) compared to MSSA in total isolates (17.5%, n = 48), respectively. However, these were 28.4% (n = 78) and 12.4% (n = 34) for MRSA and MSSA infections in women, respectively. MRSA rates per age groups of 0-20, 21-50, and >50 years of age were 15% (n = 42), 17% (n = 48), and 32% (n = 89), respectively. However, MSSA in the same age groups were 13% (n = 35), 9% (n = 25), and 8% (n = 22). Interestingly, MRSA increased proportional to age, while MSSA concomitantly decreased, implying dominance of the latter ancestors early in life and then gradual replacement by MRSA. The dominance and seriousness of MRSA despite enormous efforts in place is potentially for the increased use of beta-lactams known to enhance virulence. The Intriguing prevalence of the CA-MRSA patterns in young otherwise healthy individuals replaced by MRSA later in seniors and the dominance of penicillin-resistant MSSA phenotypes imply three types of host- and age-specific evolutionary lineages. Thus, the decreasing MSSA trend by age with concomitant increase and sub-clonal differentiation into HA-MRSA in seniors and CA-MRSA in young and otherwise healthy patients strongly support the notion of subclinal emergences from a resident penicillin-resistant MSSA ancestor. Future vertical studies should focus on the surveillance of invasive CA-MRSA rates and phenotypes.

Keywords: CA-MRSA; HA-MRSA; S. aureus epidemiology; nosocomial S. aureus.

Figure 1

Antibiogram patterns of methicillin-resistant Staphylococcus aureus isolates recovered from clinical specimens in Ha’il region, Saudi Arabia. AUG—amoxicillin */clavulanic acid (2/1); AMP—ampicillin, CTX—cefotaxime; FOX—cefoxitin, CIP—ciprofloxacin; CD—clindamycin; DAP—daptomycin, E—erythromycin; FU—fusidic acid: CN—gentamicin; IMI—imipenem, LNZ—linezolid; MXF—moxifloxacin; MUP—mupirocin; F—Nitrofuran; OX—oxacillin; P—penicillin; RD—rifampicin; TEC—teicoplanin; TE—tetracycline; SXT—trimethoprim */sulfamethoxazole; VA—vancomycin; IMLS—inducible macrolide, lincosamide, and streptogramin; LEV—levofloxacin; TGC—tigecycline; TOB—tobramycin.

Figure 2

Antibiogram patterns of methicillin-susceptible Staphylococcus aureus isolates recovered from clinical specimens in Ha’il region, Saudi Arabia AUG—amoxicillin */clavulanic acid (2/1), AMP—ampicillin, CTX—cefotaxime, FOX—cefoxitin, CIP—ciprofloxacin, CD—clindamycin, DAP—daptomycin, E—erythromycin, FU—fusidic acid, CN—gentamicin, IMI—imipenem, LNZ—linezolid, MXF—moxifloxacin, MUP—mupirocin, F—nitrofuran, OX—oxacillin, P—penicillin, RD—rifampicin, TEC—teicoplanin, TE—tetracycline, SXT—trimethoprim */sulfamethoxazole, VA—vancomycin, LEV—levofloxacin, TGC—tigecycline, TOB—tobramycin.

Figure 3

Gender differences in methicillin-resistant and susceptible Staphylococcus aureus distributions among men and women in the Ha’il region, Saudi Arabia.

Figure 4

Age-specific distributions of methicillin-resistant and susceptible Staphylococcus aureus lineages in Ha’il region, Saudi Arabia.