Open Access

Prevalence of Nasal colonization with Staphylococcus aureus in 4 cities in Peru

  • Joan Neyra1Email author,
  • Michael Ellis2,
  • Claudio Rocha1,
  • Juan Silvera3,
  • Moisés Apolaya3,
  • Maruja Bernal1,
  • Rina Meza1,
  • Enrique Canal1,
  • Yocelinda Meza1 and
  • David Blazes4
Tropical Diseases, Travel Medicine and Vaccines20162:12

https://doi.org/10.1186/s40794-016-0025-x

Received: 5 March 2016

Accepted: 7 June 2016

Published: 22 July 2016

Abstract

Background

Antimicrobial resistance (AMR) is a growing public health threat around the world and is not well characterized in the developing setting. Specifically, there is a lack of information regarding nasal colonization with S. aureus and methicillin-resistant Staphylococcus aureus (MRSA) in Latin America and Peru.

Methods

This is the report of the baseline findings of a prospective cohort study followed up over 1 year at four geographically and ecologically distinct Peruvian Air Force bases in order to determine S. aureus nasal colonization prevalence and risk factors. Additionally, all MRSA isolates underwent molecular analysis which included pulsed-field gel electrophoresis and determination of virulence and resistance genes.

Results

We enrolled 756 military personnel. Anterior nares colonization with Staphylococcus aureus was detected in 73 of 756 participants (9.7 %) and MRSA was detected in 2 of 756 (0.3 %). Colonization rates differed significantly (P = 0.02) between geographic enrollment sites: Talara-4.3 %, Iquitos-9.1 %, Arequipa-14.0 % and Lima-11.3 %. Risk factors for S. aureus colonization included being male and a reported history of respiratory disease.

Conclusion

Overall, we found low prevalence of S. aureus and MRSA nasal colonization in this Peruvian military population. These findings contribute to the overall epidemiological understanding of S. aureus and MRSA in Latin America. The colonization rates which varied based on geographical location warrants further study.

Keywords

Antimicrobial resistance Methicillin-resistant Staphylococcus aureus Military personnel

Background

The increasing prevalence of methicillin-resistant Staphylococcus aureus is a global problem, affecting military and non-military populations around the world. MRSA was first documented in 1960, and until the late 1990s, its presence was confined largely to hospital settings with occasional outbreaks. Since then, the number of outbreaks and infections caused by MRSA, specifically community–associated methicillin-resistant Staphylococcus aureus (CA-MRSA) strains increased steadily [1, 2]. USA300 genotype is the predominant CA-MRSA strain recovered from outbreak investigations in U.S. and different countries in Europe and Asia, such as Japan [3], constituting a common cause of community associated skin and soft tissue infections (SSTIs).

Nasal colonization with Staphylococcus aureus or MRSA is a risk factor for subsequent infection by these bacteria [4, 5]. In non-Latin American populations, colonization status varies with approximately 20–30 % persistently colonized and 20 % is intermittently colonized [68]. Colonization is facilitated by the anatomy of the nasal vestibule and the resistance of S. aureus to microbicide peptides in the mucus [9]. Nasal colonization appears to change during one’s lifetime. Colonization begins shortly after birth, decreases during the first 5 years and then it increases until 50 % are carriers between 6 and 12 years; and finally it decreases as children mature and become adults [10]. In the military setting, Staphylococcus aureus infections complicate combat-related injuries and produce skin and soft-tissue infections during deployments or training. Among U.S. soldiers, MRSA SSTIs represent a considerable burden, and nasal colonization is a risk factor for subsequent disease [1, 1114]. For example, the cumulative incidence of SSTIs after 10 weeks of follow-up at training facilities in U.S. military trainees was 38 % in MRSA-colonized subjects while in non-colonized it was only 2 % [11].

The Centers for Disease Control and Prevention’s (CDC) 2013 report on antibiotic resistant pathogens listed MRSA as one of the most serious threats, causing 80,461 severe infections and 11,285 deaths per year in the U.S., leading to a heavy burden of the healthcare system [15]. Similarly, the 2014 WHO Global Health Report on Antimicrobial Resistance reported that in all the WHO regions, MRSA prevalence of infections was above 20 % and increased the risk of death and the associated healthcare costs [16, 17]. In Latin America, a surveillance network for resistant bacterial infections was organized in 1998 under Pan American Health Organization (PAHO) sponsorship; collecting data from specific national and regional hospitals with adequate laboratory infrastructure and resources. However, there is little information regarding the prevalence in other areas, so the geographic extent and the characteristics of MRSA infections in Latin America are not well described in terms of prevalence, isolates, and risk factors [18]. Our current knowledge indicates that four MRSA clones are the most prevalent in Latin America: Brazilian, Pediatric, Cordobes/Chilean and New York/Japan, with marked differences in virulence, antimicrobial resistance profile and geographical distribution [19].

In Peru, current information about MRSA is mostly limited to case reports or series from hospital-based samples from reference hospitals with appropriate protocols for lab procedures and resources. Unfortunately, these studies do not inform us about the prevalence of S. aureus nasal colonization nor the epidemiological characteristics in the community, especially in young at-risk populations such as military personnel. Our work was the first study to systematically determine the prevalence and the molecular characteristics of nasal colonization with Staphylococcus aureus and MRSA among a Peruvian military population in multiple cities in Peru. Herein, we report the baseline results of this study.

Methods

Study design

We conducted a prospective cohort study with 1 year of follow-up among active duty military personnel from four bases one in each region of the Peruvian Air Force (Lima, Arequipa, Talara, and Iquitos). This is the report of the baseline findings of this cohort. The study population included male and female military active duty personnel, between age 18 and 59 years, stationed at these bases with different climate characteristics (Iquitos is located in the jungle; Talara, in the northern desert coast, Lima at the central coast with mild to warm temperatures depending on the season, and Arequipa, which is located at high altitude in the southern highlands, with a dry and relatively cold climate). See Fig. 1.
Fig. 1

Map of Peru showing the location of the four sites. Lima, the capital city of Peru is located at the central desert coast; Talara, in the northern desert coast; Arequipa, in the southern highlands; and Iquitos is located in the northeastern jungle (Image taken from Google Earth)

Study procedures

We enrolled military personnel from four large bases in each Air Force region. After we obtained written informed consent, each participant completed a self-administered questionnaire about demographic and risk factors and provided a nasal swab. Investigators obtained a sample from the vestibular area of each of the nares, using BD BBL CultureSwabs® (BD Diagnostic, Sparks MD). Each nasal swab specimen was placed in a refrigerated container and later stored in a refrigerator at 4 °C until the time of the shipping to Naval Medical Research Unit-6 lab (NAMRU-6). Once they arrived at NAMRU-6 Bacteriology lab, the time gap between sample collection and plating was 1 month.

Lab procedures

Labeled swabs were shipped to the Naval Medical Research Unit N° 6 (NAMRU-6) located at Lima, Peru. Nasal culture specimens were placed in 5 ml of tryptic soy broth (TSB) supplemented with 6.5 % NaCl and incubated for 18-24 h at 35 °C. After that time, a 75 microL aliquot was plated onto mannitol salt agar. Plates were incubated for up to 48 h at 37 °C and inspected for yellow colonies characteristic of S. aureus. Identified isolates were sub cultured onto tryptic soy agar with 5 % sheep blood. Subsequent colonies underwent catalase and coagulase testing per Micro Lab Standard Operational Procedures (SOP) at NAMRU-6. All confirmed S. aureus isolates collected from the nasal swabs were shipped to Uniformed Services University (USU)’s Laboratory where they underwent susceptibility testing using disk diffusion tests for identifying MRSA strains, following the standards established by the Clinical and Laboratory Standards Institute [20]. Additionally, all MRSA strains underwent pulsed field gel electrophoresis (PFGE) procedures. Using polymerase chain reaction (PCR) we detected Panton-Valentine Leukocidin (PVL), arginine catabolic mobile element (ACME), staphylococcal chromosome cassete (SCCmec) type, presence of toxic shock syndrome toxin (TST), gene ileS-2 for resistant to mupirocin (mupA), and tolerance to chlorhexidine (qacA/B) using standard protocols.[7].

Statistical analysis

Overall and baseline colonization status are described based on gender, rank, base of recruitment, age group, time of service in the Peruvian Air Force (≤10 years, 11–20 years, > 20 years), type of activities, smoking status, previous hospitalizations in the last 12 months, previous deployments, use of antibiotics in the last 12 months, previous SSTIs in the last 12 months, previous respiratory diseases, use of corticosteroids in the last 12 months, place of residence, medical conditions; and is reported as numbers and proportions with two-sided 95 % confidence intervals. We also report the prevalence rate of nasal colonization with MRSA strains and the results of the antimicrobial susceptibility for those isolates positive to Staphylococcus aureus. We used a logistic regression model to determine the association with the variables listed above. The Institutional Review Boards at USU (Bethesda, MD, USA), and NAMRU-6 (Lima Peru) approved the research protocol.

Results

Demographic and clinical characteristics

We enrolled 756 participants. The mean age of the participants was 30.3 ± 11.5 years, but almost 60 % of our study population was younger than 30 years. Slightly more than 80 % were male and 61 % of the participants had more than 10 years of military service. Almost 90 % of the study population included Non-Commissioned officers and troops, and their occupations included administrative (32.5 %), instructional (36.5 % and combat (29.2 %) activities. We found that 20.1 % of the participants had a reported medical condition. Of them, 10 % reported gastrointestinal diseases, 5.4 % reported a skin disease, 2.6 % reported a respiratory disease, and 1.1 % reported an infectious disease. More than a third of the participants (34.8 %) reported the use of antibiotics during the previous year; of these, 52 % (136) gave a specific antibiotic. In addition, 20.2 % reported the use of corticosteroids; and 11.6 % of the enrolled participants were hospitalized during the previous year. Regarding the diagnosis of any SSTI during the previous year, only 5.8 % reported a SSTI. Smoking was common: 34.2 % were current smokers, 16.7 % were past smokers, and 45.6 % reported never smoking (Table 1).
Table 1

Demographic characteristics of study participants

Variable

Frequency (N = 756)

Percentage (%)

Age

  

 18 – 29 years

450

59.5

 30 – 39 years

95

12.6

 40 – 49 years

151

20.0

 50 years or more

60

7.9

Time of service

  

 10 years or less

463

61.2

 11 – 20 years

103

13.6

 20 years or more

190

25.1

Sex

  

 Female

146

19.3

 Male

610

80.7

Rank

  

 Officers

84

11.1

 Non-Commissioned Officers

368

48.7

 Troops

304

40.2

Base of recruitment

  

 Iquitos

253

33.5

 Arequipa

164

21.7

 Talara

162

21.4

 Lima

177

23.4

Administrative activities

  

 No

510

67.5

 Yes

246

32.5

Instruction activities

  

 No

483

63.9

 Yes

273

36.1

Combat activities

  

 No

535

70.8

 Yes

221

29.2

Number of activities

  

 Not related

106

14.0

 Unique

580

76.7

 Multiple

70

9.3

Place of residence

  

 Barracks

250

33.1

 Inside the base

114

15.1

 Outside the base

392

51.9

Medical conditions

  

 No

604

79.9

 Yes

152

20.1

Number of medical conditions

  

 None

604

79.9

 One disease

118

15.6

 More than one disease

34

4.5

Use of antibiotics in the previous year

  

 No

427

56.5

 Yes

263

34.8

 Unknown

66

8.7

Use of corticosteroids in the previous year

  

 No

536

70.9

 Yes

153

20.2

 Unknown

67

8.9

Hospitalized during the previous year

  

 No

645

85.3

 Yes

88

11.6

 Unknown

23

3.0

Diagnosis of SSTIs during the previous year

  

 No

671

88.8

 Yes

44

5.8

 Unknown

41

5.4

Smoking status

  

 Never

345

45.6

 Past smoker

126

16.7

 Current smoker

259

34.2

Baseline nasal colonization with Staphylococcus aureus and MRSA

The baseline nasal colonization prevalence among the 756 enrolled participants was 9.7 %. There were two periods of recruitment, in October-November 2013 (655 participants) and April-August 2014 (101 participants), and the baseline nasal colonization rates for each period were similar (9.8 % vs. 8.9 %, p = 0.7853, Z-statistic for comparison of two proportions). The overall rate of colonization with MRSA was 0.3 % during the study period (2 of 756). These isolates were collected during the 6 month visit at Arequipa, one in a participant enrolled in October 2013 and a second from a different participant who was enrolled in in May 2014). Molecular analysis of these MRSA isolates demonstrated that they possessed SCCmec type IV and qacA/B (chlorhexidine tolerance), but lacked genes for PVL, mupirocin resistance, and toxic shock syndrome toxin (TST).

Table 2 shows statistically significant associations between prevalence of nasal colonization at baseline and demographic and clinical variables. Those participants between 18 and 29 years old and 40 to 49 years old had a higher prevalence of nasal colonization (10.2 % vs. 11.3 %); while, the prevalence was lower than 7 % for other age groups. Nasal colonization was greater in male than female (10.3 vs. 6.8 %, p = 0.201). The troops had 11.5 % of nasal baseline nasal colonization, higher than officers or non-commissioned officers (9.5 % vs. 8.2 %). There was a statistically significant difference in the distribution of nasal colonization by base of recruitment (p = 0.023); Talara had the lowest baseline prevalence (4.3 %) compared to the other three bases that had similar rates (Iquitos-9.1 %, Arequipa-14.0 % and Lima-11.3 %). Those who lived on base but not in the barracks had the lowest prevalence (5.3 %) but this was not significantly (p = 0.198) different from those who lived at the barracks (11.2 %) and those who lived off the base (9.9 %).
Table 2

Prevalence of baseline nasal colonization among the different variables under study (N = 756)

Variable

Baseline Nasal colonization (%, 95 % CI)

P value

Positive (n = 73)

Negative (n = 683)

Age

   

 18 – 29 years

10.2 (7.4 – 13.0)

89.8 (86.9 – 92.6)

0.537a

 30 – 39 years

6.3 (1.4 – 11.2)

93.7 (88.8 – 98.6)

 40 – 49 years

11.3 (6.2 – 16.3)

88.7 (83.7 – 93.8)

 50 years or more

6.7 (0.3 – 13.0)

93.3 (86.9 – 99.7)

Time of service

   

 10 years or less

10.6 (7.8 – 13.4)

89.4 (86.6 – 92.2)

0.334

 11 – 20 years

5.8 (1.3 – 10.4)

94.2 (89.6 – 98.7)

 20 years or more

9.5 (5.3 – 13.7)

90.5 (86.3 – 94.7)

Sex

   

 Female

6.8 (2.7 – 10.9)

93.2 (89.0 – 97.3)

0.201

 Male

10.3 (7.9 – 12.7)

89.7 (87.3 – 92.1)

Rank

   

 Officers

9.5 (3.2 – 15.8)

90.5 (84.2 – 96.8)

0.340

 Non-Commissioned Officers

8.2 (5.3 – 10.9)

91.8 (89.0 – 94.7)

 Troops

11.5 (7.9 – 15.1)

88.5 (84.9 – 92.1)

Base of recruitment

   

 Iquitos

9.1 (5.5 – 12.6)

90.9 (87.4 – 94.5)

0.023

 Arequipa

14.0 (8.7 – 19.4)

85.9 (80.6 – 91.3)

 Talara

4.3 (11.8 – 7.5)

95.7 (92.5 – 98.8)

 Lima

11.3 (6.6 – 15.9)

88.7 (84.0 – 93.4)

Number of activities

   

 Not related

10.4 (4.5 – 16.2)

89.6 (83.8 – 95.5)

0.587

 Unique

9.1 (6.8 – 11.5)

90.9 (88.5 – 93.2)

 Multiple

12.9 (4.9 – 20.8)

87.1 (79.2 – 95.1)

Number of medical conditions

   

 None

9.9 (7.5 – 12.3)

90.1 (87.7 – 92.5)

0.122

 One disease

6.1 (1.7 – 10.5)

93.9 (89.5 – 98.3)

 More than one disease

17.6 (4.6 – 30.7)

82.4 (69.3 – 95.4)

Respiratory diseases the previous year

   

 No

9.1 (7.0 – 11.2)

90.9 (88.8 – 92.9)

0.002

 Yes

30.0 (9.4 – 50.6)

70.0 (49.4 – 90.6)

Use of antibiotics the previous year

   

 No

9.1 (6.4 – 11.9)

90.9 (88.1 – 93.6)

0.598

 Yes

11.0 (7.2 – 14.8)

88.9 (85.2 – 92.8)

 Unknown

7.6 (11.3 – 14.0)

92.4 (85.9 – 98.9)

Use of dicloxacillin previous year

   

 No

9.3 (7.2 – 11.4)

90.7 (88.6 – 92.8)

0.005

 Yes

33.3 (5.4 – 61.2)

66.7 (38.8 – 94.6)

Use of corticosteroids the previous year

   

 No

8.9 (6.5 – 11.4)

91.0 (88.6 – 93.5)

0.432

 Yes

12.4 (7.2 – 17.7)

87.6 (82.3 – 92.8)

 Unknown

8.9 (2.1 – 15.9)

91.0 (84.1 – 97.9)

Hospitalized during the previous year

   

 No

9.6 (7.3 – 11.9)

90.4 (88.1 – 92.7)

0.971

 Yes

10.2 (3.8 – 16.6)

89.8 (83.4 – 96.2)

 Unknown

8.7 (0.0 – 20.5)

91.2 (79.5 – 100)

Diagnosis of SSTIs during the previous year

   

 No

9.5 (7.3 – 11.8)

90.5 (88.2 – 92.7)

0.848

 Yes

9.1 (0.5 – 17.7)

90.9 (82.3 – 99.5)

 Unknown

12.2 (5.2 – 22.4)

87.8 (77.6 – 97.9)

Smoking status

   

 Never

8.1 (5.2 – 11.0)

91.9 (88.9 – 94.8)

0.297

 Past smoker

12.7 (6.9 – 18.5)

87.3 (81.5 – 93.1)

 Current smoker

10.4 (6.7 – 14.2)

89.6 (85.8 – 93.3)

Place of residence

   

 Barracks

11.2 (7.3 – 15.1)

88.8 (84.9 – 92.7)

0.198

 Inside the base

5.3 (1.1. – 9.4)

94.7 (90.6 – 98.9)

 Outside the base

9.9 (6.9 – 12.9)

90.1 (87.1 – 93.0)

aWe used the Fisher’s exact test. For the rest of the variables, we used the Pearson chi square test

Having a respiratory disease increases the prevalence of nasal colonization (30 %) compared with those without respiratory disease (9.1 %, p = 0.002). Smoking did not affect the prevalence of nasal colonization; the rates were similar among those who never smoked (8.1 %), previous smokers (12.7 %) and currently smokers (10.4 %) (p = 0.300) (Table 3).
Table 3

Potential risk factors associated with baseline nasal colonization with Staphylococcus aureus

Variable

N

Unadjusted OR

Adjusted OR (95 % CI)

P-value

Use of antibiotics during the previous year

    

 No

400

Ref

Ref

 

 Yes

238

1.2

1.4 (0.8 – 2.6)

0.283

Hospitalization during the previous year

    

 No

566

Ref

Ref

 

 Yes

72

1.0

1.0 (0.4 – 2.4)

0.980

Diagnosis of SSTI during the previous year

    

 No

600

Ref

Ref

 

 Yes

38

0.5

0.4 (0.1 – 1.8)

0.237

Sex

    

 Female

122

Ref

Ref

 

 Male

516

1.8

2.4 (1.0 – 5.7)

0.043

Base of recruitment

    

 Talara

144

Ref

Ref

 

 Iquitos

207

2.5

2.5 (0.9 – 6.5)

0.065

 Lima

149

2.8

2.7 (0.9 – 7.3)

0.051

 Arequipa

138

3.9

4.5 (1.7 – 11.9)

0.002

Smoking status

    

 Never smoked

312

Ref

Ref

 

 Past smoker

107

1.7

1.6 (0.8 – 3.5)

0.204

 Current smoker

219

1.2

1.1 (0.6 – 2.1)

0.756

Respiratory diseases

    

 No

619

Ref

Ref

 

 Yes

19

3.5

4.5 (1.4 – 14.7)

0.014

Time of service

638

0.99

0.97 (0.94 – 0.99)

0.030

Among those who used antibiotics during the last year, the nasal colonization prevalence at baseline was not different among those who used them (11.0 %) or not (9.1 %). However, when we analyzed the use of dicloxacillin the previous year, those who reported its use had a 33.3 % prevalence of nasal colonization, compared with those who did not report its use (9.3 %, p = 0.005). Regarding the use of corticosteroids, those who used them the previous year, had a prevalence of 12.4 %, which was similar to those who did not use them (8.9 %), (p=: 0.432).

In terms of hospitalization during the previous year, the rates were similar among those who were hospitalized (10.2 %) and those who were not (9.6 %) (p = 0.971). Similarly there was no difference in prevalence between those who had the diagnosis of SSTIs during the last year (9.1 %) and those who did not (9.5 %). The identified risk factors for S. aureus colonization included being male and a reported history of respiratory disease; while time of service had a slight protective effect.

Antimicrobial susceptibility of positive isolates and MRSA isolates

NAMRU-6 and USUHS labs processed 183 positive Staphylococcus aureus samples from the participants during the study period (1 year). Antimicrobial susceptibility is reported in Table 3. The highest resistance was to erythromycin (16.4 %). In addition, 6.6 % had an inducible resistance to clindamycin. All isolates were susceptible to ceftaroline, trimethoprim-sulfamethoxazole, vancomycin, and linezolid (Table 4).
Table 4

Antimicrobial susceptibility of 183 Staphylococcus aureus isolates

Antibiotic

Number (%) of samples

Susceptible

Resistant

Intermediate

Clindamycina

179 (97.8)

4 (2.2)

-

Erythromycin

153 (83.6)

30 (16.4)

-

Doxycycline

180 (98.4)

-

3 (1.6)

Linezolid

183 (100)

-

-

Oxacillin

181 (98.9)

2 (1.1)

-

Rifampin

183 (100)

-

-

TMP-SMX b

183 (100)

-

-

Vancomycin

183 (100)

-

-

Gentamicin

177 (96.7)

6 (3.3)

-

Levofloxacin

182 (99.5)

1 (0.5)

-

Ceftaroline

183 (100)

-

-

a 6.6 % of the samples showed inducible resistance to clindamycin

bTMP-SMX, trimethoprim-sulfamethoxazole

Discussion

Baseline prevalence

There are only a few studies of nasal colonization in active duty military populations, primarily from the US and one from China, but none in Peru or Latin America. These studies found that the prevalence of colonization in American recruits was 31 % [11], while the Chinese military found a different rate depending if individuals were deployed to urban (24.6 %) or suburban military centers (16.1 %) [21]. In both cases, the prevalence was higher than what we found at baseline in our study population (9.7 %). Only two previous studies were performed in community settings in Peru. One study included only children from Cajamarca and found a prevalence of 11.9 % [22], while the second included inhabitants of an impoverished community of Lima, and found that among adults of different ages the prevalence of nasal colonization ranged from 20.4 to 39.6 % [23]. These two previous studies in Peru are comparable with others studies performed in Latin American countries that showed that the nasal colonization rates with Staphylococcus aureus in community settings was quite varied. In adult populations, the nasal colonization rates in Brazil ranged between 32.7 % [24] and 40.8 % [25]; while among Colombian medical students the rate was 25 % [26]. The prevalence we obtained in the Peruvian military was closer to the prevalence rate reported among adult students in Nigeria (14 %) and healthcare workers in Nicaragua (6.7 to 11.6 %) [27, 28]. In Peru, 3 MRSA strains from Peruvian citizens returning from abroad were characterized in 2011, one was ST30 and the other two were ST8 clones which are related to the USA300 clone [29].

We found differences in the prevalence of nasal colonization based on the site of the geographical site if study enrollment. Of the four sites, Lima is the capital city of Peru (approximately 10 million inhabitants), while Arequipa (900,000 inhabitants) and Iquitos (420,000 inhabitants) are the most important urban centers in the highlands and the jungle and had higher prevalence rates; while Talara, which is a smaller city than the other three (101,000 inhabitants), had only 4.3 %. This colonization prevalence differences may be attributed to a number of factors including climate and ecology, population size, or access to healthcare. An important aspect of population size is that it generally suggests differences in commercial movement, and therefore access to common antibiotics that are still sold without a medical prescription at small pharmacies and drugstores. Additionally, the distribution of antibiotics to each military health facility is based on the most prevalent diseases and the size of the base, which are larger in Lima, Arequipa and Iquitos where administrative and operational regional offices are located, and therefore exceed the population assigned to Talara, which is only an operational base. The increased exposure to antibiotics in Lima, Iquitos and Arequipa might favor the development of nasal colonization with Staphylococcus aureus by eliminating other commensal bacteria colonizing the human nares; unfortunately information regarding the most used antibiotics at each of the bases or local areas is currently unavailable.

Dicloxacillin is an antibiotic belonging to the beta lactam family that is used extensively for the treatment of SSTIs. We had expected that the use of dicloxacillin might reduce the rates of nasal colonization with Staphylococcus aureus, but we found the opposite. Possibly, the normal microbiota in the anterior nares is more susceptible than Staphylococcus aureus to dicloxacillin, therefore favoring the Staphylococcus aureus growth. Another possible reason can be the misuse of this antibiotic, which is usually prescribed for 7 to 14 days, but if the dose and time of prescription were not adequate, the antibiotic might have limited effect. We were not able to collect information regarding the dose, time of prescription, where the antibiotics were purchased, or if the treatment was completed.

We identified only two participants with MRSA and therefore our overall prevalence of MRSA colonization during the study period was 0.3 % (2 of 756). These isolates possessed SCCmec type IV which is the characteristic mobile genetic element carrying the mecA gene (methicillin-resistance) found most commonly in CA-MRSA strains. Our MRSA colonization prevalence was close to those reported in previous studies in Peru and Latin America, where it ranges from 0.6 to 1.8 % [23, 30, 31] in communities; however these proportions are lower than those observed in developed countries like US or Europe. In terms of military populations, our results reflect that MRSA nasal colonization is lower than rates reported in US military populations (3 %), while the Chinese study did not detect any MRSA [11, 21].

Our questionnaire was not designed to provide more specific historical information regarding the type of SSTI and treatments prescribed, dose and timing of antibiotics and corticosteroids, time of hospitalization, place, and antibiotics used during this time, which could have given us more detailed information regarding these risk factors. Also, given that this was a self-administered questionnaire, there is the potential for recall bias. In addition, it is possible that some participants did not understand the questions asked or did not know the medical terms used; therefore they left the questions blank. In addition, it is possible that sample handling could have affected the recovery of positive S. aureus isolates, specifically during the sampling procedure due to discomfort of the participants that led to movements of the head and a poor quality sample, and the limited available timeframe we had for doing it. Different climate conditions at each site may have affected also the recovery due to the use of a refrigerated container that could not have kept a low temperature at all times.

We believe our results can serve as a proxy to understanding of the nasal colonization with Staphylococcus aureus in the community. We found that these isolates have a remarkable antimicrobial susceptibility with very little resistance when compared with other populations. This susceptibility may allow us an optimization of the current treatment of different infections where Staphylococcus aureus is a common etiologic agent. This standardization should help to reduce the indiscriminate exposure to more expensive and broader spectrum antibiotics that should be left as second or third line options, which are more expensive and increase the risk of adverse reactions.

Conclusions

In summary, we found a low prevalence of baseline nasal colonization with Staphylococcus aureus (9.7 %) and MRSA (0.3 %) in an active duty military population in Peru. Our results increase the current knowledge about Staphylococcus aureus nasal colonization in Peru and Latin America. Further study exploring the geographically differences in S. aureus nasal colonization warrants further investigation.

Abbreviations

AMR, Antimicrobial resistance; MRSA, methicillin-resistant Staphylococcus aureus; SCCmec, staphylococcal cassette chromosome mec

Declarations

Acknowledgments

None.

Funding

This research was funded by the Global Emerging Infections Surveillance and Response System (GEIS) of the Armed Forces Health Surveillance Branch. Ref, Number: P0004_12_HS.

Availability of data and materials

Data will not be shared since participants belong to the Peruvian Armed Forces and it contains sensitive information.

Authors’ contributions

JN was responsible for developing the study protocol, obtaining IRB approval, overseeing the implementation of the study, coordinating and providing general oversight to all research efforts and performed data collection and analysis. DB oversaw the implementation of the study protocol as well as the manuscripts writing. ME was responsible for sample testing, sequencing and characterization of MRSA strains at USUHS. CR provided oversight of the laboratory diagnostic procedures at NAMRU-6 and helped during the sample collection at the study sites. MA was in charge of coordination with the Peruvian Air Force, provided general oversight to the data collection from all the Peruvian Air Force establishments. JS helped with the sample collection at the study sites and with the coordination for data collection of SSTIs at each health establishment. RM, YM, MB, EC performed the sample identification, molecular tests and antimicrobial susceptibility tests at NAMRU-6 Bacteriology labs. All authors read and approved the final manuscript.

Competing interests

The authors declare that they have no competing interests.

Consent for publication

We report aggregated data from the participants. During the consent process we asked for consent to publish form the participants.

Ethics approval and consent to participate

The protocol was approved by the Institutional Review Board of U.S. Naval Medical Research Unit No. 6, Lima-Peru (NAMRU-6), Ref. number NAMRU6.2013.0021.

Each study participant signed an informed consent previous to enrollment.

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Authors’ Affiliations

(1)
Naval Medical Research Unit N° 6 Lima-Peru (NAMRU-6)
(2)
University of Toledo College of Medicine and Life Sciences
(3)
Peruvian Air Force
(4)
Uniformed Services University (USU)

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Copyright

© The Author(s). 2016

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