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The nasopharyngeal bacterial flora in infancy: effects of age, gender, season, viral upper respiratory tract infection and sleeping position

Linda M. Harrison, James A. Morris, David R. Telford, Susan M. Brown, Keith Jones
DOI: http://dx.doi.org/10.1111/j.1574-695X.1999.tb01323.x 19-28 First published online: 1 August 1999

Abstract

The aim of the investigation was to determine the effect of age, gender, viral upper respiratory tract infection (URTI), season and sleeping position on the composition of the nasopharyngeal bacterial flora in infancy. Seventy-two babies, 38 male and 34 female, whose birthdates were evenly spread throughout the year were followed from birth to 18 months of age. From 0 to 6 months nasopharyngeal swabs were obtained once a month in periods without URTI and daily for 3 days during episodes of URTI. From 12 to 18 months of age nasopharyngeal swabs were obtained in the early morning after an overnight sleep and later in the day after the baby had been up for over 2 h. Swabs were obtained in prone and supine sleepers with and without infection. In infants aged 0–6 months URTI had little effect on the nasopharyngeal bacterial flora, but there was a marked effect of age and less marked effect of season and gender. In particular Staphylococcus aureus carriage decreased with age, was most common in the winter months and the density of colonisation was greater in males than females. In infants aged 12–18 months the combination of prone sleeping with URTI and an early morning swab led to increased carriage of staphylococci, streptococci, Haemophilus influenzae and Gram-negative bacilli which are not normally part of the nasopharyngeal flora. These results are relevant to sudden infant death syndrome (SIDS). The combination of prone sleeping and URTI reproduces the nasopharyngeal flora seen in SIDS. Gram-negative bacilli isolated from SIDS cases should not be dismissed as post-mortem contaminants. The features of S. aureus make it a prime candidate for a pathogenic role in SIDS.

Keywords
  • Sudden infant death syndrome
  • Nasopharyngeal bacterium
  • Prone sleeping
  • Bacterial toxin

1 Introduction

There is both theoretical and experimental evidence in support of the hypothesis that toxins produced by bacteria that commonly colonise the nasopharynx have a pathogenic role in sudden infant death syndrome (SIDS) [17]. This idea, which is reviewed elsewhere in this issue, is consistent with the key epidemiological features of SIDS including the age distribution, the winter excess of cases and the association with prone sleeping and passive smoking. There is, however, only limited information available on the composition of the normal nasopharyngeal flora in infancy and the extent to which it is influenced by factors involved in SIDS such as age, upper respiratory tract infection (URTI), gender, season and sleeping position [8, 9].

In this paper we report the results of a longitudinal study of the nasopharyngeal bacterial flora in 72 infants followed from birth to 18 months of age. A stratified design allowed us to examine the individual effects of age, gender, URTI, and season in infants aged 0–6 months. We also documented the effects of prone and supine sleeping in infants aged 12–18 months.

2 Materials and methods

2.1 Population studied

Parents were recruited to the study at ante-natal classes. The aim was to follow a minimum of two boys and two girls born in each calendar month for 12 successive months. In order to achieve this minimum over-recruitment was necessary and in all 72 babies were followed, 38 males and 34 females (Table 1). Their birthdates were evenly spread throughout the year.

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Table 1

The gender and month of birth of the babies

GenderMonth of birthTotal
JFMAMJJASOND
Boys32423435235238
Girls43242424232234
Total75665859467472

2.2 Collection of swabs

In the first 6 months of life the babies were visited at home at least once per month and a nasopharyngeal swab was obtained when the baby was free of an infection (determined clinically). The mothers were asked to report when the babies had URTI and the babies were then visited at home daily for 3 days and nasopharyngeal swabs were obtained on each occasion. At 12 months the parents were contacted and asked to report any episode of URTI. During an episode the baby was visited in the early morning (between 5 a.m. and 9 a.m.) and a nasopharyngeal swab obtained as the baby awoke from its overnight sleep. A second swab was obtained later in the day after the baby had been up and awake for over 2 h. Sixty per cent of the babies found the procedure distressing and were not revisited, but in the others the procedure of an early morning swab and a swab later in the day was repeated when the baby was free of infection.

2.3 Processing of pernasal swabs

The pernasal swabs obtained in the first 6 months of life were treated as follows. Each swab was inoculated on to a variety of bacteriological culture media which were then incubated in an appropriate atmosphere (Table 2). Plates were examined after 24 and 48 h incubation. A semi-quantitative measure of growth was made for all colony types. These were recorded, subcultured, identified and stored for further tests.

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Table 2

Bacteriological culture media and conditions of incubation for samples of nasopharyngeal secretions

Culture mediumAtmosphereTemperature (°C)Time (h)
5% Horse-blood agar5% CO23748
‘Chocolate’ blood agar5% CO23748
5% Horse-blood agar with nalidixic acid and colistin (Oxoid Staph/Strep supplement)5%CO23748
aerobic3748
7% Horse-blood agar in brain-heart infusion agar with Oxoid GC supplement5% CO23748
5% Horse-blood agar with neomycin 70 mgl−1anaerobic3748
Maconkey agaraerobic3748

The pernasal swabs obtained after 12 months of age were treated as follows. Each swab head was transferred to 0.1% buffered peptone water and vortexed for 1 min. Three blood agar and three chocolate agar plates were inoculated using a spiral plater and then incubated in 5% CO2 at 37°C for 48 h. Counts were performed on all colony types on the plates and expressed as organisms (strictly colony forming units) ml−1 of inoculum. Each colony type was recorded, subcultured and identified.

2.4 Statistical analyses

Results were analysed using SPSS software (version 6.1.4). Differences were evaluated using the χ2 test, Fisher's exact test, the Mann-Whitney U test and the Wilcoxon paired samples test.

3 Results

3.1 Characteristics of the population

The month of birth of the infants is shown in Table 1. There were 72 infants in all with 38 boys and 34 girls. The birthdates were evenly spread throughout the year and there were at least two boys and two girls born in each calendar month. The social class distribution of the parents is shown in Table 3. The distribution is similar to that of the general population.

View this table:
Table 3

The social class distribution of the parents of the babies compared with the general population in England and Wales [21] and the parents of SIDS cases [22]

Social classIIIIIInIIImIVVUnclassified
Number8191712952
Percentage11.126.423.616.712.56.92.8
General population %4.626.922.220.715.45.84.4
SIDS parents %2.110.36.721.510.32.147.2

3.2 Effect of URTI on isolation of bacteria

The parents reported 74 episodes of URTI, and in 69 of these, nasopharyngeal swabs were obtained. The age distribution of URTI (n=74) is shown in Fig. 1. There were more episodes of URTI in the autumn and winter months than in the spring and summer months (Fig. 2, P<0.01).

Figure 1

The age distribution of URTI.

Figure 2

The seasonal distribution of URTI.

The organisms isolated during episodes of URTI are shown in Table 4. For the majority of organisms there was no significant difference in isolation rate between infants with an URTI and appropriate age-, gender- and season-matched controls without URTI. (Comparisons were made between an individual infant with URTI and the same infant without URTI in the same month; an individual with URTI and its age- and gender-matched control(s) without URTI in the same month; and an individual with URTI and its age- but not gender-matched control(s) without URTI in the same month.) The only statistically significant differences found are shown in Table 5.

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Table 4

Organisms isolated during episodes of URTI

Organism%Organism%
Corynebacterium pseudodiphtheriticum41.2Streptococcus salivarius8.8
Staphylococcus aureus40.6Corynebacterium group ANF7.1
Branhamella catarrhalis39.5Streptococcus sanguis6.6
Streptococcus mitis23.6Staphylococcus haemolyticus5.5
Staphylococcus epidermidis23.0Streptococcus agalactiae4.4
Streptococcus pneumoniae17.6Escherichia coli3.3
Haemophilus influenzae10.4Neisseria lactamica3.3
  • Corynebacterium group ANF includes C. afermentans and C. propinquum.

View this table:
Table 5

The effect of URTI on nasopharyngeal bacterial carriage

OrganismURTIP value
Present n (%)Absent n (%)
S. epidermidis13 (18.8)50 (32.9)<0.05
B. catarrhalis27 (39.1)36 (23.7)<0.02
α- or non-haemolytic streptococci19 (27.5)23 (15.2)<0.05

The carriage of Staphylococcus epidermidis was increased in infants without URTI, while Branhamella catarrhalis and α- or non-haemolytic streptococci were increased in infants with URTI. The carriage of Staphylococcus aureus was increased in infants with URTI but the difference did not reach statistical significance.

3.3 Effect of age on isolation of bacteria

The effect of age over the first 6 months of life on nasopharyngeal bacterial carriage is shown in Tables 68. Table 6 shows that in infants free of URTI the carriage of staphylococci steadily falls through the first 6 months of life while the carriage of most of the other organisms rises. In Table 7 it is shown that if carriage in the first 3 months is compared with carriage over 3 months of age the differences are highly significant. In Table 8 the nasopharyngeal isolation rate for infants with URTI under and over 3 months of age is shown. In general, the trends are similar but the differences are less marked, and because the total number of swabs is less in the URTI group than the non-URTI group, many of the differences do not reach statistical significance.

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Table 6

The effect of age on nasopharyngeal bacterial carriage in the first 6 months of life

OrganismAge (months)
<1 n (%)1 n (%)2 n (%)3 n (%)4 n (%)5 n (%)6 n (%)
S. aureus44 (63.8)28 (43.8)30 (47.6)22 (33.8)23 (32.9)15 (24.2)11 (28.2)
S. epidermidis43 (62.3)28 (43.8)22 (34.9)16 (24.6)16 (22.9)14 (22.6)7 (17.9)
S. pneumoniae4 (5.8)7 (10.9)6 (9.5)15 (23.1)16 (22.9)13 (21.0)11 (28.2)
S. mitis10 (14.5)10 (15.6)12 (19.0)16 (24.6)20 (28.6)19 (30.6)12 (30.8)
C. pseudodiphtheriticum14 (20.3)19 (29.7)25 (39.7)29 (44.6)36 (51.4)28 (45.2)17 (43.6)
B. catarrhalis4 (5.8)6 (9.4)15 (23.8)12 (18.5)23 (32.9)17 (27.4)15 (38.5)
Neisseria species1 (1.4)0 (0.0)1 (1.6)5 (7.7)2 (2.9)11 (17.7)10 (25.6)
H. influenzae0 (0.0)3 (4.7)4 (6.3)7 (10.8)10 (14.3)9 (14.5)5 (12.8)
Enterobacteriaceae2 (2.9)1 (1.6)0 (0.0)1 (1.5)3 (4.3)1 (1.6)1 (2.6)
View this table:
Table 7

The number of positive cultures for infants free from infection under 3 months of age compared infants over 3 months of age

OrganismAge <3 months n (%)Age >3 months n (%)P value
S. aureus102 (52.6)71 (29.8)<0.00001
S. epidermidis92 (47.5)54 (22.7)<0.00001
S. pneumoniae17 (8.8)55 (23.1)<0.0001
S. mitis32 (16.5)67 (28.2)<0.005
α- or non-haemolytic streptococci27 (13.9)34 (14.3)NS
C. pseudodiphtheriticum57 (29.4)111 (46.6)<0.0005
B. catarrhalis24 (12.4)68 (28.6)<0.0001
Neisseria species2 (1.0)28 (11.8)<0.00005
H. influenzae7 (3.6)31 (13.0)<0.001
Enterobacteriaceae3 (1.5)6 (2.5)NS
View this table:
Table 8

The number of positive cultures for infants with an infection under 3 months of age compared to infants over 3 months of age

OrganismAge <3 months n (%)Age >3 months n (%)P value
S. aureus19 (61.3)8 (21.0)<0.001
S. epidermidis7 (22.3)6 (15.8)NS
S. pneumoniae4 (12.9)9 (23.7)NS
S. mitis10 (32.3)8 (21.0)NS
α- or non-haemolytic streptococci7 (22.6)12 (31.6)NS
C. pseudodiphtheriticum9 (29.0)16 (42.1)NS
B. catarrhalis7 (22.5)20 (52.6)<0.05
Neisseria species3 (9.7)1 (2.6)NS
H. influenzae1 (3.2)6 (15.8)NS
Enterobacteriaceae3 (9.7)1 (2.6)NS

3.4 Effect of season on isolation of bacteria

The effect of season on nasopharyngeal bacterial carriage is shown in Tables 9 and 10. The seasonal effects are not marked and in most cases the comparisons do not differ significantly. There is, however, a trend for S. aureus to be more common in the autumn and winter months in both infants with and without URTI. S. epidermidis is more common in the summer in infants without URTI.

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Table 9

A seasonal comparison of nasopharyngeal bacterial colonisation in infants free from infection

OrganismSpring n (%)Summer n (%)Autumn n (%)Winter n (%)P value
S. aureus39 (37.1)39 (34.8)45 (42.5)50 (45.9)NS
S. epidermidis26 (24.8)55 (49.1)42 (39.6)23 (21.1)<0.00005
S. pneumoniae23 (21.9)18 (16.1)13 (12.3)18 (16.5)NS
S. mitis25 (23.8)25 (22.3)25 (23.6)24 (22.0)NS
α- or non-haemolytic streptococci17 (16.2)12 (10.7)17 (16.0)15 (13.8)NS
C. pseudodiphtheriticum40 (38.1)45 (40.2)45 (42.5)38 (34.9)NS
Aerobic spore-bearing bacillus (ASB)8 (7.6)1 (0.9)2 (1.9)4 (3.7)<0.05
B. catarrhalis27 (25.7)15 (13.4)26 (24.5)24 (22.0)NS
Neisseria species18 (17.1)5 (4.5)3 (2.8)4 (3.7)<0.0001
H. influenzae7 (6.7)9 (8.0)9 (8.5)13 (11.9)NS
Enterobacteriaceae2 (1.9)1 (0.9)1 (0.9)5 (4.6)NS
  • Neisseria species include N. meningitidis, N. lactamica, N. cinerea and other organisms only identified to genus level.

View this table:
Table 10

A seasonal comparison of nasopharyngeal bacterial colonisation in infants with URTI

OrganismSpring n (%)Summer n (%)Autumn n (%)Winter n (%)P value
S. aureus3 (25.0)3 (27.3)14 (50.0)7 (38.9)NS
S. epidermidis2 (16.7)2 (18.2)5 (17.9)4 (22.2)NS
S. pneumoniae0 (0.0)2 (18.2)5 (17.9)6 (33.3)NS
S. mitis4 (33.3)3 (27.3)7 (25.0)4 (22.2)NS
α- or non-haemolytic streptococci5 (41.7)1 (9.1)9 (32.1)4 (22.2)NS
C. pseudodiphtheriticum7 (58.3)6 (54.5)9 (32.1)3 (16.7)NS
B. catarrhalis7 (58.3)6 (54.5)9 (32.1)5 (27.8)NS
Neisseria species1 (8.3)0 (0.0)0 (0.0)3 (16.7)NS
H. influenzae0 (0.0)2 (18.2)0 (0.0)5 (27.8)<0.01
Enterobacteriaceae0 (0.0)0 (0.0)2 (7.1)2 (11.1)NS

For the majority of organisms, rates of colonisation did not differ significantly between boys and girls. Females were, however, more likely to carry Corynebacterium pseudodiphtheriticum (P<0.05) and Enterobacteriaceae (P<0.05) than males, while β-haemolytic streptococci were more likely to be isolated from male infants (P<0.05). The isolation rate of S. aureus did not differ significantly between males and females, but when present males had heavier growth than females (P<0.05).

3.5 Effect of prone sleeping position on isolation of bacteria

Table 11 shows the median bacterial count and the mean number of isolates from infants aged 12–18 months sampled under a number of different conditions. To simplify description the following abbreviations are used:

  1. Regular sleeping position, prone (P) or supine (S).

  2. Presence of URTI, present (P) or absent (A).

  3. Position when sampled, prone (P), supine (S) or upright (U).

View this table:
Table 11

The effect of sleeping position and URTI on median bacterial count and the mean number of isolates from infants aged 12–18 months

ConditionsNumber of casesMean number of isolatesBacterial count (median)
Usual sleeping positionURTIPosition when sampledAbbreviation of conditions
PronePresentPronePPP273.26399 854
PronePresentUprightPPU272.4153 784
ProneAbsentPronePAP122.4190 217
ProneAbsentUprightPAU122.754 556
SupinePresentSupineSPS122.2270 061
SupinePresentUprightSPU122.3153 523
SupineAbsentSupineSAS42.025 651
SupineAbsentUprightSAU41.7540 649

The sequence of letters used to describe sampling conditions follows the order 1,2,3. For example, the abbreviation PAU describes an infant who regularly sleeps prone (P), is free from infection (A), and the pernasal swab is obtained when the infant is in the upright position (U).

The bacterial count and the number of isolates were highest in infants sleeping prone with infection who are sampled in the early morning after an overnight sleep (PPP). When the same infants with infection are sampled after being awake and up for over 2 h the bacterial count and the number of isolates were significantly less (PPP>PPU, P<0.01 for number of isolates, P<0.0001 for bacterial count). Infants sleeping prone with infection had significantly more isolates in the early morning swab than infants sleeping prone without infection (PPP>PAP, P<0.05). Infants sleeping prone with infection also had significantly more isolates in the early morning swab than infants sleeping supine with infection (PPP>SPS, P<0.01). Infants sleeping prone without infection had a higher bacterial count in the early morning swab than infants sleeping supine without infection (PAP>SAS, P<0.05). Infants sleeping supine with infection had a higher bacterial count in the early morning swab than in the swab taken when the baby is awake and upright (SPS>SPU, P<0.05). Infants sleeping supine with infection had a higher bacterial count in the early morning swab than infants sleeping supine without infection (SPS>SAS, P<0.05).

3.6 Bacterial isolates from infants

In general the combination of prone sleeping with infection and an early morning swab leads to increased isolation of most of the organisms. Gram-negative bacilli, particularly Haemophilus influenzae, were more common in prone compared with supine sleepers (P<0.01). Neisseria species were also more common in those sleeping prone (P<0.05). Table 12 shows comparisons of bacterial counts for specific organisms which differed significantly. Once again, in general the highest counts were found in those sleeping prone with URTI.

View this table:
Table 12

The effect of sleeping position and URTI on bacterial counts contained in pernasal swabs obtained from infants aged 12–18 months

OrganismComparison of conditionsEffectP value
All Gram-negative bacilli (GNB)PPP v. SPSPPP>SPS<0.05
PPP v. PAPPPP>PAP<0.05
H. influenzaePPP v. PPUPPP>PPU<0.0005
PPP v. PAPPPP>PAP<0.05
GNB other than H. influenzaePPP v. PPUPPP>PPU<0.05
All Gram-positive cocci (GPC)PPP v. PAPPPP>PAP<0.05
All streptococciPPP v. PAPPPP>PAP<0.02
All staphylococciPPP v. PPUPPP>PPU<0.05
S. pneumoniaePPP v. PPUPPP>PPU<0.02
S. mitisPPP v. PPUPPP>PPU<0.05
Gram-positive bacilli (GPB)PPP v. PAPPAP>PPP<0.05
PPU v. PAUPAU>PPU<0.02
Corynebacterium speciesPPP v. PAPPAP>PPP<0.05
PPU v. PAUPAU>PPU<0.01
B. catarrhalisPPU v. SPUSPU>PPU<0.05
  • For abbreviations see Table 11.

There was also an interaction between gender and prone sleeping in that males sleeping prone, with or without infection, had increased counts of Gram-positive cocci, including S. aureus, compared with females (P<0.05).

4 Discussion

This study was designed to determine how the composition of the nasopharyngeal bacterial flora is influenced by factors such as viral URTI, age, gender, season and sleeping position, all of which have a role in SIDS. A particular strength of the study is the stratified design with a minimum of two boys and two girls born in each calendar month and then followed for 6 months. This means that the individual effect of age, gender, URTI and season can be examined having controlled for the other three. In this study URTI was based on the mother's assessment.

The age distribution of reported URTIs (Fig. 1) was similar to the age distribution of SIDS in that both rise from birth to a peak at 2–3 months of age, but differs in that the subsequent rate of fall of URTIs is much less rapid than for SIDS. This fits with the prediction of the mathematical model of the common bacterial toxin hypothesis [1]. In essence the individual toxins implicated in the causation of SIDS are much more common (prevalent) than the individual viruses which lead to URTI. Thus infants and children will be susceptible to URTI long after they have acquired immunity to common toxins.

In infants aged 0–6 months, URTIs had only a small effect on nasopharyngeal bacterial carriage. Although there was a trend to increased nasopharyngeal carriage of a number of organisms, including S. aureus, this only reached statistical significance with B. catarrhalis and α- or non-haemolytic streptococci. S. epidermidis showed significantly decreased carriage with URTI. Infants who die of SIDS have a disturbed nasopharyngeal bacterial flora when compared with age-, gender- and season-matched healthy infants [10, 11]. The SIDS cases have increased carriage of staphylococci, streptococci and Gram-negative bacilli, including H. influenzae and Enterobacteriaceae. In this study the isolation rate of Enterobacteriaceae was low in infants aged 0–6 months with or without URTI, and viral infection did not reproduce the nasopharyngeal flora seen in SIDS.

Age did have a marked effect on nasopharyngeal bacterial carriage. There was a steady decline in the isolation rate of staphylococci from birth to 6 months of age and a steady increase in the carriage of a number of other organisms including streptococci, C. pseudodiphtheriticum, B. catarrhalis and H. influenzae. Increased carriage of S. aureus in the first 3 months of life has been noted in previous studies [8, 9, 12] and might be linked to increased expression of the Lewisa antigen in nasopharyngeal secretions at this age [1315].

The effect of season on nasopharyngeal bacterial carriage is much less marked. There is a tendency for the carriage of S. aureus to be more common in the autumn and winter when URTIs are more prevalent. This is consistent with in vitro studies, in which viral infections have been demonstrated to enhance binding of S. aureus and several Gram-negative species [16, 17]. By comparison, S. epidermidis is significantly more common in the summer months. Gender also had only a small effect in infants aged 0–6 months but it is interesting to note that growth of S. aureus was significantly heavier in boys than girls.

In the second part of the study, in infants aged 12–18 months there were a number of observations which are pertinent to SIDS and the common bacterial toxin hypothesis. A prediction of the hypothesis is that when infants sleep prone secretions will pool in the upper airways leading to increased bacterial growth and toxin production [18]. If infants sleep supine, the secretions will drain under gravity into the oesophagus and bacterial growth will be less. This postural difference will be exacerbated by URTI which causes increased production of secretions and decreased effectiveness of muco-ciliary clearance [19, 20]. The prediction therefore is that a combination of prone sleeping with URTI and an early morning swab will result in the highest bacterial count, and that is what was found (Table 11). Supine sleeping, absence of URTI and obtaining the swab when the baby is upright were associated with lower bacterial counts. In addition, the combination of prone sleeping with URTI and an early morning swab was associated with increased isolation of staphylococci, streptococci, H. influenzae and other Gram-negative bacilli. This combination effectively reproduced the nasopharyngeal bacterial flora found in SIDS. The last group of organisms, the Gram-negative bacilli which are not normally part of the nasopharyngeal flora, presumably grow in the pooled secretions but do not adhere to the mucosal surface as these organisms quickly disappear when the baby is upright. If the organisms that grow are toxigenic Enterobacteriaceae, however, the infant could be at risk of SIDS during sleep.

In the second part of the study, gender was associated with increased carriage of staphylococci, including S. aureus, in males sleeping prone.

There are a number of conclusions that derive from this investigation which are relevant to SIDS.

  1. URTI had little effect on the nasopharyngeal flora in infants aged 0–6 months and did not reproduce the flora found in SIDS, but in that part of the study, most of the infants slept supine and the swabs were often obtained when the infants were upright. In the second part of the study, however, the combination of prone sleeping with URTI and an early morning swab did reproduce the flora seen in SIDS.

  2. Prone sleeping has a marked effect on the nasopharyngeal bacterial flora and this could explain the increased risk of SIDS in infants who sleep prone. In this study prone sleeping was investigated in infants aged 12–18 months, because before 6 months of age most infants are put to sleep supine and remain so. After 6 months of age the infants were able to turn from supine to prone positions. It would be possible to investigate the effect of prone sleeping in babies under 12 months of age, but if these studies are undertaken, an early morning swab will be essential as the flora changes once the baby is upright.

  3. S. aureus emerges as the prime candidate organism for a pathogenic role in SIDS. It is common in the early months of life when SIDS reaches a peak, and isolation of the bacteria is increased in the prone sleeping position and with URTI. It is also more common in the winter months, although this did not reach statistical significance and growth is heavier in males than females. Pyrogenic toxins produced by S. aureus have been identified in SIDS infants in a previous study [3] and more recently in tissues of 33/67 (53%) SIDS infants from Scotland, France and Australia [23].

  4. The isolation of Gram-negative bacilli other than H. influenzae from the nasopharynx in SIDS is often dismissed as post-mortem contamination; but the results in this study show that Gram-negative bacilli are commonly found in the nasopharynx when prone sleeping is combined with URTI.

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View Abstract