Serotyping and antibiotic susceptibility of Streptococcus pneumoniae strains isolated in Algeria from 2001 to 2010

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Serotyping and antibiotic susceptibility of Streptococcus pneumoniae strains isolated in Algeria from 2001 to 2010 Sérotypage et sensibilité aux antibiotiques des souches de Streptococcus pneumoniae isolées en Algérie de 2001 à 2010 H. Tali-Maamar a,∗, R. Laliam a, C. Bentchouala b, D. Touati c, K. Sababou d, S. Azrou d, M. Azzam e, W. Amhis f , L. Oussadou g , R. Belouni h , F. Smati b , K. Rahal a a

Service de bactériologie médicale, institut Pasteur d’Algérie, Algiers, Algeria b Service de microbiologie, CHU Constantine, Constantine, Algeria c Laboratoire Mère–Enfant, CHU Beni Messous, Alger, Algeria d Laboratoire central SS Boufarik, Boufarik, Algeria e Laboratoire central, CHU Tizi, Ouzou, Algeria f Laboratoire central SS Bologhine, Alger, Algeria g Laboratoire central SS Birtraria, Alger, Algeria h Laboratoire central, CHU Ben Boulaïd, Blida, Algeria

Received 28 June 2011; received in revised form 14 August 2011; accepted 6 December 2011 Available online 20 January 2012

Abstract Introduction. – Pneumococcal infections are a major public health problem because of the virulence of this bacterium and its ability to develop resistance. Material and method. – Two hundred and ninety-four strains of Streptococcus pneumoniae were isolated from sterile (56.8%) and non-sterile samples (43.2%), from January 2001 to July 2010. Results. – The interpretation of antibiotic susceptibility testing, according to CLSI criteria (M100-S21 2011), yielded a 25.2% overall resistance to penicillin, with 23.5% of strains isolated from CSF (meningitis), and only 1.7% in other samples. Resistance to cefotaxime was 8.1% (including 4.4% at a high level). The most common serotypes were: 14 (19.5%), 23F (9.7%), 6B (9.3%), 19F (5.4%), and serotype 1 (5%). The percentage of these serotypes isolated from normally sterile sites in children under 5 years of age was 31.25% for 14, 10.4% for 23F, 8.3% for 19F, 6.25% for 6B, and 4.2% for serotype 1. The theoretical vaccinal coverage against invasive infections in children under 2 years of age was 61.5%, 69.2%, and 76.9% for the 7-valent, 10-valent, and 13-valent conjugate vaccines, respectively. Penicillin non-susceptible Streptococcus pneumoniae (PNSP) strains accounted for 67.1, 68.6, and 72.8% for each of these three vaccines. Conclusion. – There was a variation of serotype rates compared to previous studies. The increase in pneumococcal antibiotic resistance is concerning, particularly for the treatment of pneumococcal infections in children and infants. Pneumococcal vaccination is not compulsory yet in Algeria. © 2011 Elsevier Masson SAS. All rights reserved. Keywords: Algeria; Serotype; Streptococcus pneumoniae; Vaccine

Résumé Introduction. – Les infections pneumococciques représentent un problème majeur de santé publique, en raison de la virulence du germe et de sa capacité à développer des résistances. Matériel et méthode. – De janvier 2001 à juillet 2010, nous avons collecté 294 souches de Streptococcus pneumoniae, provenant de sites stériles (56,8 %) et non stériles (43,2 %). Résultats. – L’interprétation des tests de sensibilité aux antibiotiques, selon les critères du CLSI (M100-S21 2011), a montré un taux de résistance à la pénicilline de 25,2 %, dont 23,5 % de souches isolées de LCR (cas de méningites), alors que dans les autres sites de prélèvement, ce taux ∗

Corresponding author. E-mail addresses: [email protected], [email protected] (H. Tali-Maamar).

0399-077X/$ – see front matter © 2011 Elsevier Masson SAS. All rights reserved. doi:10.1016/j.medmal.2011.12.001

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était de 1,7 %. La résistance au céfotaxime était de 8,1 % (dont 4,4 % de haut niveau). Les sérotypes les plus fréquents étaient : 14 (19,5 %), 23F (9,7 %), 6B (9,3 %), 19F (5,4 %) et le sérotype 1 (5 %). La fréquence de ces sérotypes dans les sites normalement stériles chez l’enfant de moins de cinq ans, était : 14 (31,25 %), 23F (10,4 %), 19F (8,3 %), 6B (6,25 %) et pour le sérotype 1 (4,2 %). La couverture vaccinale théorique des infections invasives chez l’enfant de moins de deux ans, était de 61,5 %, 69,2 % et 76,9 % pour les vaccins polysaccharidiques conjugués héptavalent, décavalent et 13 valences respectivement. Les souches de pneumocoques de sensibilité diminuée à la pénicilline représentaient 67,1 %, 68,6 % et 72,8 % pour chacun de ces trois vaccins. Conclusion. – Il y avait une variation de la fréquence des sérotypes comparativement aux études précédentes. L’augmentation de la résistance du pneumocoque aux antibiotiques est inquiétante, en particulier pour la prise en charge des infections pneumococciques de l’enfant et du nourrisson. La vaccination antipneumococcique n’est pas obligatoire en Algérie. © 2011 Elsevier Masson SAS. Tous droits réservés. Mots clés : Algérie ; Streptococcus pneumoniae ; Sérotypes ; Vaccin

1. Introduction Streptococcus pneumoniae is a commensal bacterium of the nasopharyngeal tract in humans. It is usually responsible for ENT infections in children, most often acute otitis media. Severe infections may occur, especially in individuals with a weakened immune system who may present with pneumonia, meningitis, and or bacteremia [1]. Children under 2 years of age are the most exposed to these infections. In developing countries, the WHO estimates at more than three million the yearly death rate due to pneumonia, and mainly to the pneumococcus [2]. It is also the first etiology of purulent meningitis in children [3]. Pneumococcus virulence is related to composition and quantity of capsular antigens expressed by the strain. Ninety serotypes are documented for the pneumococcus; some are frequently isolated during infectious episodes, because of their invasive virulence factor, whereas others are more commonly responsible for carriage [1,4]. The pneumococcus is naturally susceptible to ß-lactams; strains with decreased susceptibility to penicillin were reported in the 1960s. Since that period, resistance to this agent and other antibiotics has been constantly increasing, at various degrees from one region to another. It is also influenced by pressure of selection, and thus prescription habits. Furthermore, the phenotypic expression of this resistance, sometimes heterogeneous, makes it even more difficult to manage severe pneumococcal infections [5,6]. The diversity of serotypes, and the increasing resistance to antibiotics, are two essential elements which must be taken into account for the prevention and management of pneumococcal infections. There are two types of vaccines, polysaccharide nonconjugated (PNC) and polysaccharide conjugated (PC). The 23-valent PNC vaccine was the first to be marketed in the USA in 1983 [7]. The PC vaccines were developed in the 1990s, with 7, 9, 10, 11, and 13 valences. They trigger an immune response in children under 2 years of age, thanks to the association of capsular polysaccharides and proteins, which induces a type T-dependent immune response, the predominant form of protection in infants, which is not the case for the 23-valent antipneumococcal vaccine. They target the most frequent serotypes

in children during invasive infections, especially meningitis. These serotypes are usually the most resistant to usual antibiotic therapy. Prevenar-7® (Wyeth) has been used since 2000 in several countries. Using this vaccine has considerably decreased the number of invasive pneumococcal infections (meningitis, bacteremia); nevertheless several authors have reported the emergence of non-vaccinal serotypes in nasopharyngeal carriage, with resistance to penicillin [8–10]. The conjugated vaccines Prevenar-13® with 13 valences (Pfizer) and Synflorix® with 10 valences (GSK) have been approved since 2009 in Europe. In Algeria, the death rates due to respiratory infections and to meningitis account for respectively 36.3 and 4.4% of all deaths related to transmissible diseases (National Public Health Institute). The antipneumococcal vaccination is not listed in the vaccinal schedule. Little data has been published on S. pneumoniae strains isolated in this country [11–13]. We studied the serotypes and susceptibility to antibiotics of S. pneumoniae strains isolated in several Algerian districts, and consequently tried to find the necessary arguments to choose a vaccinal and therapeutic strategy.

2. Material and method 2.1. Bacterial strains We collected 294 non-repetitive S. pneumoniae strains for our study, from January 2001 to July 2010, in various regions of Algeria (Fig. 1). These isolates were sampled from: CSF (n = 111); blood culture (n = 41); ascitic, pleural, peritoneal, and gastric fluid (n = 15); nasal, pharyngeal, and auricular swabs (n = 73); bronchial aspiration (n = 31); and pus (n = 23) (Table 1). Among these strains, 45.6% were isolated from children among whom 33.3% in patients under 5 years of age. The strains were identified routine tests, screening for alpha hemolysis, optochin susceptibility, and sodium deoxycholate lysis. All strains were frozen and kept at −80 ◦ C, in glycerol. Nevertheless, some were difficult to maintain and we lost 38 (12.9%).

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61

Table 1 Distribution of strains according to type of sampling and age. Distribution des souches par type de prélèvement et par âge.

Sterile samples (56.8%) CSF Blood culture Puncture fluida Total Non-sterile samples (43.2%) Bronchial aspiration Auricular swab Other samplesb Total

< 2 years

2 to 5 years

32 3 3 38

11 3

8 18 6 32

6 to 10 years

11 to 15 years

> 15 years

NS

Total

7 1

14

6 1 1 8

8

23 19 7 49

32 14 4 50

111 41 15 167

2 3 9 14

2 5 8 15

1 1 3 5

15 1 25 41

3 6 11 20

31 34 62 127

NS: not specified. a Pleural fluid, peritoneal fluid, ascitic fluid, and gastric fluid. b Nasal swab, throat swab, conjunctival swab, pus, fistula, catheter.

2.2. Susceptibility to antibiotics Antibiotic susceptibility was determined by disk diffusion antibiogram, according to recommendations issued by the Clinical and Laboratory Standards Institute (CLSI) [14], on 5% sheep blood Mueller Hinton agar. The antibiotic tested was: erythromycin, chloramphenicol, tetracyclin, cotrimoxazole, levofloxacin, and vancomycin. MICs were systematically determined for ß-lactams, penicillin, amoxicillin (except for strains isolated from CSF), cefotaxim, and imipenem. The technique used was dilution in liquid medium: horse blood, Mueller Hinton as recommended by the CLSI (14). The reference strain S. pneumoniae ATCC 49619 was used for quality control.

Fig. 1. Geographic distribution of strains. Distribution géographique des souches.

We separated strains isolated from CSF from others, for the interpretation of betalactam susceptibility results, as recommended by the CLSI [14,15]. 2.3. Determination of serotypes Serotyping was performed with the latex particle agglutination (Pneumo Test Latex Statens Serum Institute), and with the capsule inflation test and monovalent serums (Statens Serum Institute). Serotyping was made on 256 strains out of the 294 collected because of conservation problems mentioned above. 3. Results Two hundred and ninety-four strains were analyzed, 56.8% from otherwise sterile sites and 43.2% from non-sterile sites; 45.5% were collected from children, 73.1% of these were under 2 years of age (Table 1); 14.6% of strains were isolated from children under 5 years of age presenting with meningitis. The ß-lactam susceptibility study yielded a global resistance rate (R + I) to penicillin of 25.2%, 6.6% for amoxicillin, and 8.1% for cefotaxim (Table 2). The analysis of results by type of sample was that 23.5% of strains isolated from meningitis were resistant to penicillin, compared to only 1.7% in samples isolated from other infected sites. The penicillin MIC50% was estimated at 0.12 ␮g/ml and 0.5 ␮g/ml, for strains isolated from CSF and bronchial aspirations. It was 0.063 ␮g/ml for strains isolated from blood cultures and ear pus. More than 75% of pneumococci non-susceptible to penicillin (PNSP) strains, presented resistance to ß-lactams and to other antibiotic classes (Fig. 2). The rate of resistance to other antibiotics was 31% for erythromycin, 30% for tetracyclin, and 43% for cotrimoxazole. Only 5.8% of strains were resistant to chloramphenicol. The most frequent serotypes were: 14 (19.5%), 23F (9.7%), 6B (9.3%), 19F (5.4%), and 1 (5%). The rate of these serotypes in sterile sites was 22.7% for 14, 13% for 23F, 5.2% for 6B, 3.8% for 19F, and 6.4% for type 1.

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H. Tali-Maamar et al. / Médecine et maladies infectieuses 42 (2012) 59–65 PEN SXT

The rate of serotypes 6A and 7F was respectively 0.7 and 1.2%. They were isolated mostly in children. The rate of serogroup 9 was 2.7%. The seven isolated strains were type 9 N and collected from normally sterile sites (n = 6) and bronchial sites (n = 1). No serotype 9 V strain was identified. The rate of serogroup 8 was 3.1%. Seven of the eight strains isolated were collected from normally sterile sites, including five from CSF. This serotype was described in 1994, among predominant types [13]. Serogroup 35 was identified in eight pneumococcal strains, among the four collected from normally sterile sites, including one PDSP. This serogroup, especially type 35B, is considered as potentially emergent [8]. Serogroup 24 was identified in seven strains, among which six from CSF and hemocultures, including four with decreased susceptibility to penicillin. The authors of an Italian study [39], reported isolating type 24F PSDP strains in patients presenting with meningitis; the genetic study of these isolates a proved their clonal similarity with type 14 strains.

27.00%

PEN

23.00%

PEN E TET SXT

18.90%

PEN E TET

8.10%

PEN E C TET SXT

8.10%

PEN E SXT

6.70%

PEN E C SXT

2.60%

PEN TET

2.60%

PEN TET SXT

1.30%

PEN C TET

1.30%

PEN C SXT

0.00%

PEN C TET SXT

0.00%

PEN C

0.00%

PEN E C TET

0.00%

PEN E C

0.00%

PEN E

0.00%

PEN: penicillin; ERY: erythromycin; TET: tetracycline, CHL: chloramphenicol, SXT: co-trimoxazole

Fig. 2. Percentage of phenotypes of resistance to five. Pourcentage des phénotypes de résistance à cinq.

4. Discussion There was a significant difference of resistance to penicillin among strains isolated from patients presenting with meningitis (23.5%) and those isolated in case other infection (1,7%) (Chi2 > 35, P ≤ 0.05). S. pneumoniae’s susceptibility to ß-lactams varied considerably depending on break points used. Resistance was much higher in strains isolated in CSF than in other types of infections (such as: ENT infections, pneumonia, and or septicemia). For the latter, the threshold MIC to detect the strains de pneumococci resistant was 4 ␮g/ml, much too high for an effective treatment of meningitis. The break points for pneumococcal ßlactam susceptibility, took into account pharmacodynamic and pharmacokinetic parameters for this class of antibiotics [14–17].

The rate of these serotypes in invasive infection was 14 (31.25%), 23F (10.4%), 19F (8.3%), 6B (6.25%) and the serotype 1 (4.2%) in children under 5 years of age. Vaccinal serotypes strains (PC vaccines) accounted for more than 70% of strains isolated from invasive infection samples in children less than 5 years of age (Figs. 3 and 4). Five of the 256 serotyped strains were type 3 (1.9%), with only one isolated from CSF in a child less than 5 years of age. This serotype is usually isolated in adults and older children [32]. Serotype 19A was identified for four strains (1.5%), among the three isolated during invasive infections, including a case of meningitis in a 10-month-old infant.

15

15

10

1

1

1

1

1

28

29

35

13

2

21

1

24

1

20

2

10

2

8

19F

1

9N

5

23F

18

14

7F

2 0 9V

1 6B

1 6A

0

1 5

3 1 3

0

1

2

4

19A

5

4

Number of strains

20

VPC-7: 4, 6B, 9V, 14, 18C, 19F, 23F VPC-10: 4, 6B, 9V, 14, 18C, 19F, 23F, 1, 5, 7F VPC-13: 4, 6B, 9V, 14, 18C, 19F, 23F, 1, 3, 5, 6A, 7F, 19A

Fig. 3. Distribution of serotypes for strains isolated from invasive samples in children 0 to 5 years of age (n = 49). Répartition des sérotypes des souches isolées de prélèvements invasifs chez l’enfant de 0 à 5 ans (n = 49).

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63

15

10

5 3 2 1 0 35

0

NS

1 29

24

20

0 21

10

8

0 9N

23F

19F

19A

1

28

1 0

18

0 14

0 7F

6B

2

1

1

0 5

3

0 4

0 1

0

1

9V

1

2

13

2

6A

Number of strains

13

NS: not specified

Fig. 4. Distribution of serotypes for PSDP strains isolated from invasive samples in children 0 to 5 years of age (n = 32). Répartition des sérotypes des souches de PSDP isolées de prélèvements invasifs chez l’enfant de 0 à 5 ans (n = 32).

The previously reported rate of S. pneumoniae resistance to ßlactams in strains isolated in Algeria [11,13] cannot be compared with our results, because criteria were different. Nevertheless, the MIC 50 (and 90) ranged from 0.032 (and 2) ␮g/ml [11] to 0.12 (and 2) ␮g/ml for penicillin. For cefotaxim, it ranged from 0.016 (and 0.5) ␮g/ml [11] to 0.032 (and 1) ␮g/ml in our study. No vancomycin or levofloxacin resistance was detected (Fig. 2). Glycopeptides and fluoroquinolones are rarely used for pneumococcal infections in Algeria [10,18–20]. But there was a significant increase (Chi2 ) of resistance for the other classes of antibiotics compared to the 2000 study, where resistance rates of 21.7, 4.6, 26.4, and 25.7% were reported for respectively erythromycin, chloramphenicol, tetracyclin, and cotrimoxazole [11]. The rates of resistance reported in 1994 [13] were very low: 16% for erythromycin, 14% for tetracyclin, 8% for cotrimoxazole, and no resistance for chloramphenicol. The rate of resistance to antibiotics was similar to the one found in other African countries [21] Nevertheless, the authors of a recent study carried out in Senegal in 2008 [22] report a weak rate of resistance to erythromycin (8,6%). The rate of serotypes is comparable to those reported recently in Tunisia, Morocco, and other countries [5,23–26]. Four serotypes were more frequent among PDSP: 14, 23F, 6B, and 9 N. The same serotypes were reported in a French study [27]. The rate of isolation of serotypes 1 and 5 was low, compared to the rate of strains isolated in 1996 and 2000 [11]. The authors of the study carried out in 1989 and 1992 [13] had reported a rate of 38% for type 1 strains; serotype 5 had rarely been isolated. In sub-Saharan countries, these serotypes are infrequent in Tunisia, whereas in Morocco type 5 is one of the predominant serotypes in young children [23,26]. In 2007, serotype 1 was the most frequently isolated in invasive infections in children in France [10]. In other countries, especially the USA and Spain, the rate of serotypes significantly fluctuated [6,28]. In Spain, the authors of a comparative study carried out in 1979 and 2007, reported important variations in the rate of serotype 1, in time [29].

Clustered cases of serotype 1 pneumococcal meningitis have been described [30,31]. Serotype 19A has been reported in au Morocco [23], Egypt [33], Kuwait [34], and in other countries where it was mentioned as a major cause of invasive infections especially in children [34–37]. This serotype was described as emergent especially in developed countries where antipneumococcal vaccination, with the heptavalent PNC vaccine, was used early [10,29,37,38]. The theoretical vaccinal coverage for PNC in children under 5 years of age is evaluated at 62.1, 66.7, and 72.4% for heptavalent, decavalent, and 13 valent vaccines respectively. Pour the children under 2 years of age this coverage is respectively 61.5, 69.2, and 76.9%. These PNC vaccines include serotypes most commonly reported as invasive in young children. Our results yield the first microbiological data S. pneumoniae, for several areas of Algeria. The results of antibiotic resistance testing showed that penicillin and amoxicillin kept their indication for the treatment of non-meningeal pneumococcal infections. The determination of MICs for ß-lactams, remains necessary in case of invasive infections, for which choosing a third generation cephalosporin as first line treatment would be wiser. The rate of resistance of strains isolated from CSF, to penicillin (23.5%) and cefotaxime (4.7% including 2.7% at high level) are alarming. The consumption of antibiotics in Algeria is based mainly on ß-lactams. Oral cephalosporins are widely used in community practice [12]. Numerous authors have reported the variation in time of circulating S. pneumoniae serotypes. The difference noted between the two studies in Constantine (1994) and Algiers (2000), and ours stress the need to implement surveillance of pneumococcal infections and pneumococcal carriage in Algeria. Efforts will be necessary to increase the number of samplings and their quality. Disclosure of interest The authors declare that they have no conflicts of interest concerning this article.

64

0.25 – 0.5 2 0.5 0.032 – 0.032 0.125 0.032

0.032

1 0 1 3 0 5 (1.7%)

4.4%

0 2 0 2 1 5 (1.7%)

3.7% 91.9%

40 13 33 26 61 173 (58.8%)

References

1 – 1 4 2 2 171 (93.4%) 6 (3.3%) 6 (3.3%)

2 2 1 1 0 6 (3.3%) 38 13 32 26 62 171 (93.4%)

2

0.5 – 0.5 2 1

24.5% 0.7% 74.8% All types included

NS: not specified; ND: break points not defined. a Pleural fluid, peritoneal fluid, ascitic fluid, and gastric fluid. b Nasal swab, throat swab, conjunctival swab, pus, fistula, catheter.

0.12

0.063 – 0.063 0.5 0.125 0 0 1 2 0 3 (1%) 40 15 33 28 62 178 (60.5%) Other than CSF Blood culture (n = 41) Other sterile samplesa (n = 15) Ear (n = 34) Bronchial aspiration (n = 31) Other non-sterile samplesb (n = 62) Total (n = 183)

1 0 0 1 0 2 (0.7%)

2 69 (23.5%) 0.12 ND 42 (14.2%) CSF (meningitis) CSF (n = 111)

MIC 50% R I

We would like to thank all microbiologists who contributed to the study by sending pneumococcal strains. Especially: A. S. Merad (Algiers), Kassah-Laouar (Batna), S. Ameur (Algiers), H. Ammari (Algiers), M. Naïm (Algiers), S. Bekkhoucha (Oran).

0.032 – 0.032 0.5 0.064 0.064 1 0 1 4 0 6 (3.3%)

MIC 50% R I S S

MIC 90%

Amoxicillin Penicillin

Table 2 Rate of Streptococcus pneumoniae (n = 294) resistance to penicillin, amoxicillin, and cefotaxim. Fréquence de la résistance de Streptococcus pneumoniae (n = 294) à la pénicilline, amoxicilline et au céfotaxime.

1

2 8 (2.7%) 0.063 6 (2%) 97 (33%)

MIC 50% R S MIC 90%

Cefotaxim

Acknowledgments

I

MIC 90%

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