Literature DB >> 20671944

Temporal Variations among Invasive Pneumococcal Disease Serotypes in Children and Adults in Germany (1992-2008).

Matthias Imöhl1, Ralf René Reinert, Mark van der Linden.   

Abstract

Nationwide surveillance of invasive pneumococcal disease has been conducted in Germany since 1992. From 1992 to 2008, a total of 12,137 isolates from invasive pneumococcal disease were collected. Data on serotypes were available for 9,394 invasive isolates. The leading serotypes were serotypes 14 (16.5%), 3 (8.0%), 7F (7.6%), 1 (7.3%), and 23F (6.0%). Variations in serotype distribution over the years are particularly extensive, especially concerning serotype 14 (min 7.4%, max 33.5%) with the highest percentages among the isolates serotyped from around 1997 to 2006. Serotypes 1 and 7F increased over the last decade. No increase was observed concerning serotype 19A. Higher pneumococcal conjugate vaccine coverages were observed among children (7v, 57.3%; 10v, 72.8%; 13v, 83.5%) than among adults (7v, 39.9%; 10v, 55.5%; 13v, 73.5%). The temporal variations in serotype distribution have to be kept in mind when interpreting vaccine coverages reported in epidemiological studies.

Entities:  

Year:  2010        PMID： 20671944      PMCID： PMC2910462          DOI： 10.1155/2010/874189

Source DB:  PubMed          Journal:  Int J Microbiol


1. Introduction

Streptococcus pneumoniae is one of the most important pathogens in bacterial pneumonia, sepsis, and meningitis worldwide [1]. Significant temporal [2-4] and regional [5-7] variations among pneumococcal serotypes have been described. While the “epidemic” serogroups (serogroups 1-3 and 5) decreased considerably in the United States during the last century, the serogroups included in the seven-valent pneumococcal conjugate vaccine (PCV7) increased clearly [2]. A similar trend has been described in Spain, where the prevalence of PCV7 serotypes increased significantly (except serotype 4) since the start of the study in the early 1980s but then decreased considerably in the 2000s for all PCV7 serotypes except serotype 23F. Among the “epidemic” serotypes, a significant decrease of serotypes 1 and 5 has been observed in the 1980s followed by a significant increase in the late 1990s, while serotype 3 decreased continuously during the observational period. Furthermore, serotypes 6A, 7F, and 19A increased significantly since the late 1990s [4]. The widespread use of antibiotics and the increasing application of pneumococcal conjugate vaccines (a general recommendation of pneumococcal conjugate vaccination for children <2 years in Germany was issued at the end of July 2006) will have an impact on future changes in serotype distribution. The NRCS has conducted surveillance for invasive pneumococcal disease in Germany since 1992 [8]. Between 1992 and 1996 surveillance was based on a limited number of laboratories in Germany on a voluntary basis [9]. In 1996, nationwide population-based surveillance of IPD in children was started [10]. This surveillance system was extended to adults in one federal state (North-Rhine Westphalia) in 2001 [11] and successively broadened to nationwide surveillance until 2009. The aim of this study was to evaluate the serotype distribution of S. pneumoniae among the isolates with invasive pneumococcal disease (IPD) that were sent to the German National Reference Center for Streptococci (NRCS) between 1992 and 2008, analyze temporal trends, and calculate the vaccine coverages for the 7-valent, 10-valent, and 13-valent pneumococcal conjugate vaccines.

2. Materials and Methods

2.1. Study Design

In this study data about invasive disease caused by Streptococcus pneumoniae in children (<16 years) and adults (≥16 years) in Germany were included using the data sources described above. Cases from January 1, 1992 to December 31, 2008 were included in this study. A case of IPD was defined by the isolation of S. pneumoniae from a normally sterile site.

2.2. Microbiological Investigations

Isolates were identified using standard procedures including bile solubility and optochin sensitivity. As a control strain, Streptococcus pneumoniae ATCC 49619 was used. Pneumococcal isolates were serotyped by the Neufeld's Quellung reaction using type- and factor-specific antisera (Statens Serum Institut, Copenhagen, Denmark). Among isolates of adults, high levels of resistance were a main trigger for initiation of serotyping during the early years of this study. Since cross-reactive serotypes were not included in the calculation, coverage information strictly refers to the serotypes included in the vaccines. Serogroup 6 isolates were not tested with respect to serotype 6C.

3. Results

A total of 12,137 isolates from invasive pneumococcal disease were collected between January 1, 1992 and December 31, 2008. The total numbers of cases for each year varied between 297 and 2,037 cases (median: 505 cases). Data on serotypes were available for 9,394 isolates (77.4% of all invasive isolates; 31.4% children, 68.6% adults; 54.9% male, 43.7% female, 1.4% no information on gender). The serotype distribution of the years 1992–2008 is shown in Table 1(a). The leading serotypes were serotypes 14 (16.5%), 3 (8.0%), 7F (7.6%), 1 (7.3%), and 23F (6.0 %). Concerning the epidemic serotypes 1–3 and 5, a slight increase was noticed during the last years, reaching levels around 20% among children and adults in 2008 (Figures 1(a)–1(c)). Variations in serotype distribution over the years are partly extensive, especially concerning serotype 14 (min 7.4%, max 33.5%) (Figure 2(a)). Differences in serotype distribution among children and adults are shown in Tables 1(b) and 1(c). The amount of serotyped isolates among all pneumococcal isolates sent to the NRCS in Germany is shown in Table 2. Over the years the percentage of isolates serotyped increased continuously and in the last four years of the study almost all isolates were serotyped.
Figure 1

(a) Distribution of the epidemic serotypes 1, 2, 3, and 5 in percent (1992–2008, n = 9,394) in all age groups. (b) Distribution of the epidemic serotypes 1–3 and 5 among children in percent (1992–2008, n = 2,948). (c) Distribution of the epidemic serotypes 1–3 and 5 among adults in percent (1992–2008, n = 6,446).

Figure 2

(a) Distribution of the 7-valent pneumococcal conjugate vaccine serotypes and the 7-valent vaccine coverage in percent (1992–2008, n = 9,394). (b) Distribution of the 7-valent pneumococcal conjugate vaccine serotypes and the 7-valent vaccine coverage among children in percent (1992–2008, n = 2,948). (c) Distribution of the 7-valent pneumococcal conjugate vaccine serotypes and the 7-valent vaccine coverage among adults in percent (1992–2008, n = 6,446).

Table 2

Distribution of isolates serotyped among pneumococcal isolates sent to the NRCS in Germany (1992–2008).

Isolates serotyped1992(%)1993(%)1994(%)1995 (%)1996 (%)1997 (%)1998 (%)1999 (%)2000 (%)2001 (%)2002 (%)2003 (%)2004 (%)2005 (%)2006 (%)2007 (%)2008 (%)
children
serotyped (%)92,282,996,665,438,792,997,696,896,2100,099,699,2100,0100,0100,0100,0100,0
serotyped (n)4729281712158161182200239258244265316287273232
total5135292631170165188208239259246265316287273232
adults
serotyped (%)42,517,217,230,431,628,729,522,926,638,652,369,368,297,7100,099,9100,0
serotyped (n)1937453100845462535416522538427058862816541805
Total45442930932926618821023120342843055439660262816551805
overall
serotyped (%)47,522,224,033,032,359,259,556,161,860,670,178,580,998,5100,099,9100,0
serotyped (n)240103811179621222323525440448362853590491519272037
total50546433835529735837541941166768980066191891519282037
Serotype 14 is considerably more frequent among children (22.5%) than among adults (13.7%). Overall, an increase of serotype 14 can be noticed from around 1997 to 2006 (Figure 2(a)). A high percentage of serotype 14 isolates remain in existence for a longer time among children (1999–2006, Figure 2(b)) than among adults (1999–2001, Figure 2(c)). Serotype 1 and serotype 7F have been clearly increasing over the last approximately 10 years, both among children and among adults. While for children the percentage of serotypes 1 and 7F reach the highest values during this study in 2008, among adults they are high, but still within the range already noted before (Figures 3(a)-3(c)). Serotype 3 is far more common among adults (10.2%) than among children (3.3%) (Tables 1(b)-1(c)). The increase observed during the last years seems to be slightly higher among adults than among children (Figures 4(a)–4(c)). Concerning serotype 19A no clear change in frequency can be observed during the period under study (Figures 4(a)–4(c)).
Figure 3

(a) Distribution of the additional 10v-pneumococcal conjugate vaccine serotypes 1, 5, and 7F and the 10-valent vaccine coverage in percent (1992–2008, n = 9,394). (b) Distribution of the additional 10v-pneumococcal conjugate vaccine serotypes 1, 5, and 7F and the 10-valent vaccine coverage among children in percent (1992–2008, n = 2,948). (c) Distribution of the additional 10v-pneumococcal conjugate vaccine serotypes 1, 5, and 7F and the 10-valent vaccine coverage among adults in percent (1992–2008, n = 6,446).

Figure 4

(a) Distribution of the additional 13v-pneumococcal conjugate vaccine serotypes 3, 6A, and 19A and the 13-valent vaccine coverage in percent (1992–2008, n = 9,394). (b) Distribution of the additional 13v-pneumococcal conjugate vaccine serotypes 3, 6A, and 19A and the 13-valent vaccine coverage among children in percent (1992–2008, n = 2,948). (c) Distribution of the additional 13v-pneumococcal conjugate vaccine serotypes 3, 6A, and 19A and the 13-valent vaccine coverage among adults in percent (1992–2008, n = 6,446).

Variations in serotype distribution also affect theoretical vaccine coverages. The overall serotype coverage for the 7-valent conjugate vaccine was 45.4% during 1992–2008. For the 10-valent vaccine and the 13-valent vaccine the overall coverages were 60.9% and 76.6%, respectively. Generally, higher coverages were observed among children (7v, 57.3%; 10v, 72.8%; 13v, 83.5%) than among adults (7v, 39.9%; 10v, 55.5%; 13v, 73.5%). Among children, the coverage of the 7-valent vaccine decreased from 64.2% in 2005 to 24.6% in 2008 (Figure 2(b)), while for adults the coverage declined to a lesser extent (2005, 45.9%; 2008, 31.2%) (Figure 2(c)). Temporal changes of the additional 10-valent and 13-valent pneumococcal vaccine serotypes and the corresponding vaccine coverages are shown in Figures 3(a)–3(c) (10v) and Figures 4(a)–4(c) (13v). Since the general recommendation of pneumococcal conjugate vaccination for children <2 years in Germany at the end of July 2006 a percentage increase among the new (10v) or upcoming (13v) vaccine serotypes was noticed especially for serotypes 1 and 7F in children (Figure 3(b)) and for serotype 3 in adults (Figure 4(c)). In comparison, coverages of the 23-valent polysaccharide vaccine are very similar among children (min, 69.0%; max, 92.3%) and adults (min, 71.0%; max, 92.6%) from 1992 to 2008 (Figure 5).
Figure 5

Coverage of the 23v-pneumococcal polysaccharide vaccine for children (n = 2,948), adults (n = 6,446), and overall (n = 9,394).

4. Discussion

In this paper we present the results of 17 years of surveillance concerning serotypes of invasive pneumococcal disease in Germany. In the present study serotype 14 was the most prevalent serotype among children, followed in frequency by the serotypes 1, 6B, 19F, 23F, and 7F, respectively. These data are similar to those published for German children previously [12, 13] and in line with data from England [14], Belgium [15], and Denmark [16]. Among adults, the most frequent serotypes were 14, 3, 7F, 1, 4, and 23F (sorted in descending order). These results are similar to a previous study from the NRCS among adults in North-Rhine Westphalia, Germany, between 2003 and 2006 [17], and are generally in line with results reported from other countries [6, 15, 18–20]; however, they deviate in part from older German data [12, 21]. The variation of serotype 14 over the years is extensive in our study with an increased prevalence from about 1997 to 2006, reaching maximum values in 2000. Although the rate of serotyped isolates among adults was low from 1999 to 2001 (1999, 22.9%; 2000, 26.6%; 2001, 38.6%), the increase seems plausible. First, the increase among adults is paralleled by an increase among children, where nearly all isolates have been serotyped. Second, the rate of isolates serotyped among adults is within the range serotyped in the years before 1999, where a similar increase of serotype 14 was not observed. Furthermore, similar data have been shown in a report from Spain [4]. Also, a small rise in frequency of serotype 14 has been reported from Denmark in 1995–1999 [16], and data from England demonstrated a rise in incidence in 2000 and 2001 [14]. The rise of serotypes 1 and 7F for nearly one decade is similar to results from Spain [4]. Concerning serotype 19A, the highest prevalences were observed in 1996 (8.3%) and 1998 (6.2%) among children, and in 1999 (7.5%) and 2000 (7.4%) among adults. Although there seems to be a slight upward movement during the years 2002 to 2008, the prevalences still are below the maximum values reported. The increase of serotype 19A reported from other countries [4, 22, 23] has not been found in Germany so far. Although changes in the incidence of different serotypes have been reported, the reasons for this are not fully understood [14]. Potential reasons discussed are changes in socioeconomic conditions, antibiotic use and resistance levels, immunocompromised status of populations, precise age distributions of the populations studied and increased life expectancy, and blood-culturing rates [2, 6, 24]. Since the general recommendation of pneumococcal conjugate vaccination for children <2 years in Germany at end of July 2006 a reduction in the percentage of IPD caused by the 7-valent vaccine serotypes was observed [25]. This effect is more apparent among children, but also present among the adult population. Similar results have been reported from other countries [3, 4, 26–29]. Logically, the percentage decrease in vaccine serotypes is paralleled by a percentage increase in the amount of IPD caused by nonvaccine serotypes, which was most prominent for serotypes 1 and 7F in children and serotype 3 in adults in this study. Serotype coverage for the 7-valent conjugate vaccine in Germany was 45.4% from 1992 to 2008. Calculated coverages for the 10-valent vaccine and 13-valent vaccine are 60.9% and 76.6%, respectively. These data are comparable to those previously reported [5, 14, 30, 31]. Coverages of all three vaccine formulations in our study are approximately 15% (7v, 17.4%; 10v, 17.3%; and 13v, 10.0%) higher among children than among adults. Differences in age distribution among study populations are known to have a major impact on vaccine coverage of the current and proposed vaccines for different age groups and, furthermore, comparable data have been published [14]. Nevertheless, some factors and limitations must be regarded when interpreting the results of this study. First of all, the isolates were sent by the participating laboratories on a voluntary basis, as participation in surveillance is not mandatory in Germany. Furthermore, the systematic sampling of invasive isolates from adults (1992) and children (1997) was taken up at different points of time, and the included population-based studies in three German federal states started in 2001 (North Rhine-Wesphalia) and 2006 (Bavaria and Saxony). Among isolates of adults, high levels of resistance were a main trigger for initiation of serotyping during the early years of this study. Therefore, the isolates may not be fully representative of all IPD in Germany over the last two decades. Moreover, the structure of the surveillance project has been continousely improved over the 15 years and, in particular, after the general recommendation of pneumococcal conjugate vaccine for children <2 years in Germany at the end of July 2006 an increased disease awareness by both clinical micobiologists and pediatricians was observed [32]. Ongoing nationwide surveillance is necessary to observe further developments of pneumococcal serotype distribution in Germany.

(a) Serotype distribution of IPD in Germany (1992–2008, n = 9,394) in all age groups.

Sero-type1992 (%)1993(%)1994 (%)1995 (%)1996 (%)1997 (%)1998 (%)1999 (%)2000 (%)2001 (%)2002 (%)2003(%)2004 (%)2005 (%)2006 (%)2007(%)2008(%)Total(%)Total(n)
148.812.67.48.513.516.517.529.833.525.221.322.823.018.819.313.38.916.51,549
37.12.93.76.09.44.22.74.32.84.06.66.74.97.56.410.511.78.0755
7F6.72.94.94.35.27.52.72.14.33.75.87.39.06.48.08.710.47.6718
17.55.81.24.33.19.45.85.56.76.44.35.36.96.97.98.58.87.3690
23F8.39.76.28.59.46.18.58.96.37.78.55.14.96.96.84.94.36.0559
47.511.74.95.12.15.27.23.43.93.54.37.54.96.06.25.64.65.4507
6B3.37.87.46.86.38.05.86.83.17.76.85.75.27.14.83.72.54.8449
19F6.71.99.96.83.15.24.97.77.16.95.23.85.45.44.54.53.44.8447
9V4.21.08.66.08.32.83.16.45.52.23.35.35.64.85.15.13.64.5425
6A6.75.84.98.53.15.25.42.64.33.53.54.63.92.83.14.94.64.3401
18C4.64.96.21.71.06.66.73.87.54.54.32.93.63.43.62.33.03.5326
19A0.82.91.21.75.22.45.83.44.33.01.41.62.62.94.34.04.23.4320
22F1.32.93.70.02.10.50.90.00.00.71.01.01.53.03.02.93.02.2208
82.11.90.00.92.10.50.90.00.41.52.32.12.12.52.22.53.02.2208
10A1.71.03.72.62.11.41.30.91.61.72.50.62.21.51.91.92.21.8172
9N2.11.01.23.41.01.40.91.31.61.21.71.31.31.41.62.02.61.8172
11A2.51.91.21.74.21.40.40.90.00.20.61.81.51.31.11.72.51.6149
12F2.51.92.51.76.31.41.31.30.02.21.01.80.70.40.41.01.71.3118
24F2.11.01.20.91.00.51.81.30.82.00.61.31.50.71.20.91.81.2116
23A0.81.01.20.00.00.91.30.00.80.50.80.80.20.40.81.01.70.988
15B0.81.90.00.01.00.00.90.91.20.00.60.30.91.10.91.01.20.983
35F0.80.01.20.90.00.50.40.90.80.50.00.30.00.40.50.71.80.874
33F1.31.01.20.90.00.91.80.90.00.50.61.00.90.70.20.60.90.768
380.40.02.50.00.00.90.40.00.40.50.60.60.70.20.30.41.40.661
51.30.02.50.92.11.40.90.90.00.20.80.20.40.40.50.40.70.655
15C1.70.00.01.70.03.80.00.00.40.00.40.60.40.60.90.50.30.653
15A0.00.00.01.70.00.01.81.70.00.71.20.80.70.60.50.10.40.548
9A0.41.01.20.92.10.90.90.00.83.52.10.60.00.40.00.20.00.547
200.81.92.50.00.00.00.00.40.00.00.00.60.60.80.30.60.40.543
NT0.00.00.00.01.00.00.00.40.00.20.20.00.70.40.30.70.50.440
17F0.01.90.00.90.00.00.90.00.00.01.20.30.70.80.30.40.20.439
16F0.00.00.01.71.00.50.00.40.01.00.60.50.40.20.40.10.40.434
33A0.00.00.00.00.00.00.00.00.00.00.00.00.40.80.80.50.20.330
310.80.01.20.90.00.00.00.00.00.50.40.50.00.10.30.10.50.326
18A0.00.01.20.00.00.00.00.00.00.50.40.60.20.20.10.30.20.222
340.80.00.00.00.00.00.40.00.00.00.40.30.20.20.20.30.20.222
rough0.01.01.20.91.00.00.00.00.40.51.01.30.00.00.00.00.00.220
23B0.01.00.00.00.00.50.40.00.00.50.00.20.40.10.10.10.20.217
9L0.00.00.00.00.00.00.40.00.00.70.80.30.20.00.20.20.00.217
130.02.90.00.00.00.90.00.00.00.20.60.00.20.00.00.10.10.215
18F0.41.90.00.90.00.50.00.90.00.00.20.20.00.10.00.30.00.215
20.41.01.20.90.00.50.00.40.00.00.00.00.00.00.00.40.00.113
12A0.00.00.00.00.00.50.00.40.00.00.20.00.20.00.30.20.00.112
28A0.00.00.00.00.00.50.00.00.40.00.40.20.00.10.10.20.00.112
35B0.00.00.00.00.00.00.00.00.00.00.20.00.20.00.00.20.20.111
10B0.00.00.00.00.00.00.40.00.00.00.00.00.20.20.00.20.10.110
Others⋆ 2.91.92.57.73.10.54.91.71.21.50.61.60.61.30.31.70.91.4130
Total1001001001001001001001001001001001001001001001001001009,394
Not sero-typed52.577.876.067.067.740.840.543.938.239.429.921.519.11.50.00.10.022.62,743

NT: nontypeable; n: number of isolates tested.

Others⋆ includes the serotypes (number of isolates): 15F (9), 18B (9), 12B (8), 7C (8), 33B (7), 10F (6), 11B (6), 11F (6), 35A (6), 19C (5), 29 (5), 37 (5), 21 (4), 24A (4), 28F (4), 35C (4), 19B (3), 22A (3), 36 (3), 45 (3), 7A (3), 24B (2), 25F (2), 39 (2), 48 (2), 6 (2), 7B (2), 12 (1), 17A (1), 18 (1), 19 (1), 23 (1), 35 (1), 9 (1).

(b) Serotype distribution of IPD in Germany (1992–2008, n = 2,948) in children (<16 years).

Sero-type1992(%)1993(%)1994 (%)1995 (%)1996 (%)1997 (%)1998(%)1999(%)2000(%)2001(%)2002(%)2003(%)2004 (%)2005(%)2006 (%)2007(%)2008(%)Total(%)Total(n)
1412.86.914.35.916.715.218.026.931.525.526.727.030.626.325.413.95.622.5664
12.13.43.60.00.09.55.66.68.08.45.44.56.07.610.512.512.97.9234
6B6.413.80.011.88.38.96.27.73.57.58.97.87.210.86.67.04.37.3216
19F8.53.47.123.50.06.36.88.88.09.65.45.76.87.38.08.44.77.2213
23F10.63.47.111.816.77.07.58.25.57.910.56.14.96.68.76.22.66.9204
7F2.13.40.05.90.07.63.72.25.54.65.88.67.96.07.79.913.86.9204
18C8.510.317.90.00.08.98.74.98.06.35.85.73.85.46.65.15.66.2182
6A14.920.73.65.90.05.15.62.74.53.84.74.93.83.51.44.85.64.4130
9V4.33.414.311.88.32.52.57.14.02.12.34.14.25.13.13.31.33.7108
46.410.37.111.88.35.17.53.84.02.13.53.73.02.83.12.20.43.5102
34.33.43.65.90.03.81.93.83.02.93.13.31.51.92.45.95.63.396
19A0.03.40.00.08.31.96.22.23.52.51.62.03.02.53.84.04.73.190
10A2.10.00.00.00.00.60.01.11.52.11.60.42.31.92.82.23.41.751
24F4.33.40.00.00.00.02.51.61.02.10.82.51.90.61.41.12.21.544
15B0.00.00.00.00.00.00.61.11.00.00.40.40.81.30.72.22.20.926
15C2.10.00.00.00.04.40.00.00.00.00.40.80.41.31.40.42.20.926
9N0.00.00.00.00.00.00.61.11.50.80.41.61.50.31.00.41.70.926
382.10.03.60.00.00.60.60.00.50.40.80.40.80.30.00.73.90.823
15A0.00.00.00.00.00.01.21.60.00.41.21.60.80.61.00.00.40.721
22F0.00.07.10.00.00.60.60.00.00.81.21.20.80.60.30.41.30.721
9A0.00.00.00.00.01.30.60.01.03.81.90.80.00.00.00.00.00.721
50.00.03.60.08.31.91.21.10.00.00.80.00.80.90.30.00.90.619
80.00.00.00.00.00.61.20.00.50.41.20.40.80.90.70.40.40.618
33F0.00.00.00.00.01.31.90.50.00.41.20.80.40.00.00.41.30.617
12F2.10.03.60.00.00.00.61.10.01.70.00.00.80.00.00.41.70.516
11A0.00.00.00.08.31.90.00.50.00.00.41.20.00.00.31.10.90.515
23A2.10.00.00.00.00.61.20.00.50.00.40.40.00.00.70.41.70.514
18A0.00.00.00.00.00.00.00.00.00.80.80.80.40.00.00.40.90.310
35F0.00.00.00.00.00.00.60.51.00.00.00.00.00.30.30.41.30.310
NT0.00.00.00.00.00.00.00.50.00.00.00.01.50.30.00.70.90.310
33A0.00.00.00.00.00.00.00.00.00.00.00.00.41.30.70.40.40.39
rough0.03.40.00.00.00.00.00.00.50.80.81.20.00.00.00.00.00.39
17F0.00.00.00.00.00.01.20.00.00.00.00.00.80.30.00.40.90.38
16F0.00.00.00.00.00.60.00.00.00.80.40.00.00.30.00.00.90.27
18B0.00.00.00.08.30.01.20.50.50.00.00.00.00.60.00.00.00.27
23B0.03.40.00.00.00.60.60.00.00.00.00.40.40.00.00.00.40.26
342.10.00.00.00.00.00.60.00.00.00.00.00.40.30.00.70.00.26
18F0.00.00.00.00.00.60.01.10.00.00.40.00.00.00.00.40.00.25
200.00.00.00.00.00.00.00.50.00.00.00.40.40.30.00.40.00.25
9L0.00.00.00.00.00.00.00.00.00.40.80.40.00.00.30.00.00.25
Others⋆ 2.13.43.65.98.32.52.51.61.50.80.80.41.51.60.33.33.01.750
Total1001001001001001001001001001001001001001001001001001002,948
Not sero-typed7.817.13.434.661.37.12.43.23.80.00.40.80.00.00.00.00.02.472

NT: nontypeable; n: number of isolates tested.

Others⋆ includes the serotypes (number of isolates): 28A (4), 11B (3), 12A (3), 12B (3), 13 (3), 33B (3), 35B (3), 15F (2), 19C (2), 21 (2), 24A (2), 28F (2), 29 (2), 35A (2), 37 (2), 7A (2), 10F (1), 19B (1), 2 (1), 31 (1), 35 (1), 35C (1), 36 (1), 39 (1), 6 (1), 7C (1).

(c) Serotype distribution of IPD in Germany (1992–2008, n = 6,446) in adults (≥16 years).

Sero-type1992(%)1993(%)1994(%)1995 (%)1996(%)1997(%)1998(%)1999(%)2000(%)2001 (%)2002 (%)2003(%)2004(%)2005(%)2006(%)2007 (%)2008 (%)Total(%)Total(n)
147.814.93.89.013.120.416.139.640.724.815.120.115.614.816.613.29.413.7885
37.82.73.86.010.75.64.85.71.95.510.78.98.110.58.311.212.510.2659
7F7.82.77.54.06.07.40.01.90.02.45.86.510.06.68.18.59.98.0514
18.86.80.05.03.69.36.51.91.93.63.15.77.86.56.77.88.37.1456
47.812.23.84.01.25.66.51.93.75.55.39.96.77.77.66.15.26.3405
23F7.812.25.78.08.33.711.311.39.37.36.24.44.87.05.94.74.55.5355
9V4.10.05.75.08.33.74.83.811.12.44.46.07.04.66.15.43.94.9317
6A4.70.05.79.03.65.64.81.93.73.02.24.44.12.43.84.94.54.2271
19F6.21.411.34.03.61.90.03.83.73.04.92.64.14.42.93.83.33.6234
6B2.65.411.36.06.05.64.83.81.97.94.44.43.35.14.03.22.33.6233
19A1.02.71.92.04.83.74.87.57.43.61.31.32.23.14.54.04.13.6230
82.62.70.01.02.40.00.00.00.03.03.63.13.33.42.92.83.42.9190
22F1.64.11.90.02.40.01.60.00.00.60.90.82.24.34.13.33.32.9187
9N2.61.41.94.01.25.61.61.91.91.83.11.01.12.01.92.32.72.3146
18C3.62.70.02.01.20.01.60.05.61.82.71.03.32.42.21.82.72.2144
11A3.12.71.92.03.60.01.61.90.00.60.92.13.02.01.41.82.72.1134
10A1.61.45.73.02.43.74.80.01.91.23.60.82.21.41.41.82.01.9121
12F2.62.71.92.07.15.63.21.90.03.02.22.90.70.70.61.11.71.6102
23A0.51.41.90.00.01.91.60.01.91.21.31.00.40.70.81.11.71.174
24F1.60.01.91.01.21.90.00.00.01.80.40.51.10.71.10.81.71.172
35F1.00.01.91.00.01.90.01.90.01.20.00.50.00.50.60.81.91.064
15B1.02.70.00.01.20.01.60.01.90.00.90.31.11.01.00.81.10.957
33F1.61.41.91.00.00.01.61.90.00.60.01.01.51.00.30.60.90.851
201.02.73.80.00.00.00.00.00.00.00.00.80.71.00.50.60.40.638
380.00.01.90.00.01.90.00.00.00.60.40.80.70.20.50.31.10.638
51.60.01.91.01.20.00.00.00.00.60.90.30.00.20.60.50.70.636
17F0.02.70.01.00.00.00.00.00.00.02.70.50.71.00.50.40.20.531
NT0.00.00.00.01.20.00.00.00.00.60.40.00.00.50.50.70.50.530
15A0.00.00.02.00.00.03.21.90.01.21.30.30.70.50.30.10.40.427
15C1.60.00.02.00.01.90.00.01.90.00.40.50.40.20.60.50.10.427
16F0.00.00.02.01.20.00.01.90.01.20.90.80.70.20.60.10.40.427
9A0.51.41.91.02.40.01.60.00.03.02.20.50.00.70.00.20.00.426
311.00.01.91.00.00.00.00.00.01.20.90.80.00.20.50.10.50.425
33A0.00.00.00.00.00.00.00.00.00.00.00.00.40.50.80.50.20.321
340.50.00.00.00.00.00.00.00.00.00.90.50.00.20.30.20.20.216
130.04.10.00.00.00.00.00.00.00.61.30.00.40.00.00.10.20.212
18A0.00.01.90.00.00.00.00.00.00.00.00.50.00.30.20.20.10.212
20.50.01.91.00.01.90.01.90.00.00.00.00.00.00.00.40.00.212
9L0.00.00.00.00.00.01.60.00.01.20.90.30.40.00.20.20.00.212
23B0.00.00.00.00.00.00.00.00.01.20.00.00.40.20.20.10.20.211
rough0.00.01.91.01.20.00.00.00.00.01.31.30.00.00.00.00.00.211
10B0.00.00.00.00.00.01.60.00.00.00.00.00.40.30.00.20.20.210
18F0.52.70.01.00.00.00.00.00.00.00.00.30.00.20.00.20.00.210
12A0.00.00.00.00.00.00.00.00.00.00.40.00.00.00.50.20.10.19
28A0.00.00.00.00.00.00.00.00.00.00.90.30.00.00.20.20.00.18
35B0.00.00.00.00.00.00.00.00.00.00.00.00.00.00.00.20.20.18
15F0.50.00.01.00.00.00.01.90.00.00.40.30.40.00.00.10.00.17
7C0.50.00.01.00.00.00.00.00.00.00.00.30.00.20.00.00.20.17
11F0.50.00.00.00.00.00.00.00.00.00.00.00.00.00.00.30.00.16
10F0.50.00.00.00.01.90.00.00.00.00.00.30.00.00.00.10.10.15
12B0.00.00.00.00.00.00.00.00.00.60.00.00.00.00.00.20.00.15
Others⋆ 1.02.71.96.01.20.08.10.00.01.80.41.60.00.90.30.80.60.958
Total1001001001001001001001001001001001001001001001001001006,446
Not sero-typed57.582.882.869.668.471.370.577.173.461.447.730.731.82.30.00.10.029.32,671

NT: nontypeable; n: number of isolates tested.

Others⋆ includes the serotypes (number of isolates): 33B (4), 35A (4), 11B (3), 19C (3), 22A (3), 29 (3), 35C (3), 37 (3), 45 (3), 18B (2), 19B (2), 21 (2), 24A (2), 24B (2), 25F (2), 28F (2), 36 (2), 48 (2), 7B (2), 12 (1), 17A (1), 18 (1), 19 (1), 23 (1), 39 (1), 6 (1), 7A (1), 9 (1).

  30 in total

1.  Emergence of macrolide and penicillin resistance among invasive pneumococcal isolates in Germany.

Authors:  Ralf René Reinert; Adnan Al-Lahham; Maria Lemperle; Christoph Tenholte; Claudia Briefs; Stefan Haupts; Hans Hubert Gerards; Rudolf Lütticken
Journal:  J Antimicrob Chemother       Date:  2002-01       Impact factor: 5.790

2.  Serotype replacement and multiple resistance in Streptococcus pneumoniae after the introduction of the conjugate pneumococcal vaccine.

Authors:  Robertino Mera; Linda A Miller; Thomas R Fritsche; Ronald N Jones
Journal:  Microb Drug Resist       Date:  2008-06       Impact factor: 3.431

3.  Capsular types and antibiotic susceptibility of Streptococcus pneumoniae isolated from patients with systemic infections in West Germany.

Authors:  A Kaufhold; R Lütticken; J Henrichsen
Journal:  Eur J Clin Microbiol       Date:  1987-12       Impact factor: 3.267

4.  Antimicrobial resistance and type distribution of Streptococcus pneumoniae isolates causing systemic infections in Germany, 1992-1994.

Authors:  R R Reinert; A Queck; A Kaufhold; M Kresken; R Lütticken
Journal:  Clin Infect Dis       Date:  1995-12       Impact factor: 9.079

5.  Increased prevalence of pediatric pneumococcal serotypes in elderly adults.

Authors:  Daniel R Feikin; Keith P Klugman; Richard R Facklam; Elizabeth R Zell; Anne Schuchat; Cynthia G Whitney
Journal:  Clin Infect Dis       Date:  2005-07-11       Impact factor: 9.079

6.  Pneumococcal bacteraemia in Belgium (1994 2004): the pre-conjugate vaccine era.

Authors:  Johan Flamaing; Jan Verhaegen; Jos Vandeven; Nadine Verbiest; Willy E Peetermans
Journal:  J Antimicrob Chemother       Date:  2007-11-13       Impact factor: 5.790

7.  Reduction in the incidence of invasive pneumococcal disease after general vaccination with 7-valent pneumococcal conjugate vaccine in Germany.

Authors:  Simon Rückinger; Mark van der Linden; Ralf René Reinert; Rüdiger von Kries; Florian Burckhardt; Anette Siedler
Journal:  Vaccine       Date:  2009-05-09       Impact factor: 3.641

8.  [Serotypes and antibiotic sensitivity of Streptococcus pneumoniae (pneumococci) in the cologne area (1980-1982)].

Authors:  R Lütticken; A Kaufhold
Journal:  Immun Infekt       Date:  1985-05

9.  Invasive pneumococcal disease in children: geographic and temporal variations in incidence and serotype distribution.

Authors:  Willam P Hausdorff
Journal:  Eur J Pediatr       Date:  2002-10-01       Impact factor: 3.183

10.  Childhood invasive pneumococcal disease in Germany between 1997 and 2003: variability in incidence and serotype distribution in absence of general pneumococcal conjugate vaccination.

Authors:  Simon Rückinger; Rüdiger von Kries; Ralf René Reinert; Mark van der Linden; Annette Siedler
Journal:  Vaccine       Date:  2008-05-05       Impact factor: 3.641
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  11 in total

1.  Modeling the cost-effectiveness of infant vaccination with pneumococcal conjugate vaccines in Germany.

Authors:  Alexander Kuhlmann; J-Matthias Graf von der Schulenburg
Journal:  Eur J Health Econ       Date:  2016-02-23

2.  Incidence of pneumococcal infections among children under 15 years in southern Catalonia throughout the heptavalent conjugate vaccine era, 2002-2009.

Authors:  A Vila-Corcoles; O Ochoa-Gondar; A Guzman-Avalos; F Gomez-Bertomeu; E Figuerola-Massana; X Raga-Luria; C de Diego-Cabanes; A Gutierrez-Perez; A Vila-Rovira; M Rodriguez-Fernandez
Journal:  Infection       Date:  2012-09-30       Impact factor: 3.553

3.  Pneumococcal carriage and antibiotic resistance in young children before 13-valent conjugate vaccine.

Authors:  Peter C Wroe; Grace M Lee; Jonathan A Finkelstein; Stephen I Pelton; William P Hanage; Marc Lipsitch; Abbie E Stevenson; Sheryl L Rifas-Shiman; Ken Kleinman; M Maya Dutta-Linn; Virginia L Hinrichsen; Matthew Lakoma; Susan S Huang
Journal:  Pediatr Infect Dis J       Date:  2012-03       Impact factor: 2.129

4.  Penicillin susceptibility breakpoints for Streptococcus pneumoniae and their effect on susceptibility categorisation in Germany (1997-2013).

Authors:  M Imöhl; R R Reinert; P M Tulkens; M van der Linden
Journal:  Eur J Clin Microbiol Infect Dis       Date:  2014-06-15       Impact factor: 3.267

Review 5.  Systematic evaluation of serotypes causing invasive pneumococcal disease among children under five: the pneumococcal global serotype project.

Authors:  Hope L Johnson; Maria Deloria-Knoll; Orin S Levine; Sonia K Stoszek; Laura Freimanis Hance; Richard Reithinger; Larry R Muenz; Katherine L O'Brien
Journal:  PLoS Med       Date:  2010-10-05       Impact factor: 11.069

6.  Bacterial spectrum of spontaneously ruptured otitis media in the era of pneumococcal conjugate vaccination in Germany.

Authors:  Mark van der Linden; Matthias Imöhl; Andreas Busse; Markus Rose; Dieter Adam
Journal:  Eur J Pediatr       Date:  2014-08-30       Impact factor: 3.183

7.  Macrolide susceptibility and serotype specific macrolide resistance of invasive isolates of Streptococcus pneumoniae in Germany from 1992 to 2008.

Authors:  Matthias Imöhl; Ralf René Reinert; Christina Mutscher; Mark van der Linden
Journal:  BMC Microbiol       Date:  2010-11-25       Impact factor: 3.605

8.  Laboratory surveillance of invasive pneumococcal disease in New South Wales, Australia, before and after introduction of 7-valent conjugate vaccine: reduced disease, but not antibiotic resistance rates.

Authors:  S Oftadeh; H F Gidding; G L Gilbert
Journal:  Epidemiol Infect       Date:  2012-09-25       Impact factor: 4.434

9.  Whole Genome Sequencing of 39 Invasive Streptococcus pneumoniae Sequence Type 199 Isolates Revealed Switches from Serotype 19A to 15B.

Authors:  Oliwia Makarewicz; Marie Lucas; Christian Brandt; Leonie Herrmann; Andreas Albersmeier; Christian Rückert; Jochen Blom; Alexander Goesmann; Mark van der Linden; Jörn Kalinowski; Mathias W Pletz
Journal:  PLoS One       Date:  2017-01-03       Impact factor: 3.240

10.  Recombinant plants provide a new approach to the production of bacterial polysaccharide for vaccines.

Authors:  Claire M Smith; Stephen C Fry; Kevin C Gough; Alexandra J F Patel; Sarah Glenn; Marie Goldrick; Ian S Roberts; Garry C Whitelam; Peter W Andrew
Journal:  PLoS One       Date:  2014-02-03       Impact factor: 3.240
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