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Group B Streptococcal Infections in a Northern Region of Italy

^a Dipartimento Materno-Infantile, Unità Operativa di Assistenza Neonatale, Università di Modena e Reggio, Emilia, Italy
^b Centro per la Valutazione dell'Efficacia dell'Assistenza Sanitaria CeVEAS, Azienda USL, Modena, Italy
^c Unità per le Malattie Batteriche Sistemiche e Respiratorie, Istituto Superiore di Sanità, Rome, Italy
^d Unità Operativa di Terapia Intensiva Neonatale, Ospedale Maggiore, Bologna, Italy
^e Unità Operativa di Terapia Intensiva Neonatale, Azienda Ospedaliero-Universitaria, Parma, Italy
^f Unità Operativa di Terapia Intensiva Neonatale e Pediatrica, Ospedale Civile M. Bufalini, Cesena, Italy
^g Unità Operativa di Terapia Intensiva Neonatale, Ospedale Infermi, Rimini, Italy
^h Unità Operativa di Pediatria e Neonatologia, Azienda USL, Imola, Italy
ⁱ Istituto Clinico di Pediatria Preventiva e Neonatologia, Ospedale S Orsola, Bologna, Italy

	ABSTRACT

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BACKGROUND. Group B streptococcus is a leading cause of neonatal bacterial infections. Despite adoption of preventive strategies, cases of infection continue to occur and there is concern that widespread antimicrobial prophylaxis might delay rather than prevent disease onset, increasing the rates of late-onset diseases.

OBJECTIVES. The purpose of this study was to determine the incidence and clinical features of early- and late-onset group B streptococcus disease in a northern region of Italy where a screening-based approach had been proposed.

METHODS. A population-based study was prospectively conducted in Emilia-Romagna, Italy. Infections that occurred during 2003–2005 in infants aged <3 months were analyzed.

RESULTS. Among 112933 live births, 56 cases of invasive disease (30 early- and 26 late-onset disease) were observed, giving an annual group B streptococcus disease incidence of 0.50 per 1000 live births. Eleven infants with early-onset disease showed no signs of illness or were mildly ill, whereas 19 had moderate-to-severe symptoms, and culture-proven meningitis was found in 2. Risk factors were detected in 12 women. Twenty-two mothers had antenatal screening; 5 were group B streptococcus colonized, but 17 were culture-negative. Prophylaxis was administered in 3 women. Three infants with late-onset diseases were mildly ill, whereas 23 had moderate-to-severe symptoms. Risk factors were found in 7 mothers. Late-onset diseases were clinically more severe than early-onset diseases; meningitis was diagnosed in 12 infants, and 4 of 26 died.

CONCLUSIONS. The incidence of early-onset disease was low. Some early infections were still observed because of negative screening results or missed opportunity for prevention. Late-onset diseases accounted for most meningitis cases and deaths. Strict adherence to protocols and adoption of optimal culture methods would further improve prevention of early-onset disease, but the aim of future strategies should be the prevention of all invasive diseases.

Key Words: sepsis • group B streptococcus • prevention • intrapartum chemoprophylaxis

Abbreviations: GBS—group B streptococcus • EOD—early-onset disease • LOD—late-onset disease • IAP—intrapartum antibiotic chemoprophylaxis • RF—risk factor • ROM—prolonged rupture of membranes

Group B streptococcus (GBS) is a leading cause of sepsis, pneumonia, and meningitis in infants. It can result in death or long-term disabilities, including mental retardation and hearing or vision loss. The disease can occur within the first 6 days of life (early-onset disease [EOD]) or later, between 1 week and 2 to 3 months of age (late-onset disease [LOD]).¹ EOD (but not LOD) is largely preventable through the administration of antibiotics in labor (intrapartum antibiotic chemoprophylaxis [IAP]). With a screening-based approach, IAP is offered to women who are GBS colonized in late pregnancy or to women with clinical risk factors (RFs) such as GBS bacteriuria during pregnancy or with a previous infant with GBS infection. With a risk-based approach, IAP is offered to women with RFs as those mentioned above or preterm delivery (<37 weeks' gestation), prolonged rupture (18 hours) of membranes (ROM), or maternal temperature 38°C during delivery.^2–4

In the United States, EOD incidence varies from 0.76 to 5.46 per 1000 live births.⁵ Between 1993 and 2004, following the wider use of IAP, the incidence dropped in selected areas of the United States from 1.7 to 0.34 per 1000 live births. In contrast, LOD changed slightly between 1996 and 2004, averaging 0.35 per 1000 live births.^{6, 7}

There are limited data in Europe on GBS disease and its preventive strategies. In most countries, the prevalence of women's GBS carriage varies between 10% and 20%, and the incidence of neonatal disease ranges from 0.5 to 2.0 per 1000 live births.⁸ Racial or socioeconomic factors, culture methods, definitions of invasive disease (probable or proven sepsis), and data collection sources (regional or national) may all explain these differences.

There was no area-based study available in Italy before the era of prophylaxis. In a small case series, the rate of EOD incidence ranged from 0.9 to 3.0 per 1000 live births, ^{9, 10} whereas only inconsistent data are available on LOD. Recommendations for prevention were endorsed by the Italian Society for Perinatal Medicine in 1996, but they have not been revised or implemented since then. A culture screening was recommended, but unlike the Centers for Disease Control and Prevention guidelines, rectal swab and the use of selective broth media were not suggested.¹¹

In 2001, a GBS Prevention Working Group was set up in Emilia-Romagna, a northern region of Italy with a population of 4500000 and 37000 live births per year. The working group promoted common prevention strategies among birth centers through twice-yearly meetings¹²; an increasing number of clinicians, microbiologists, and epidemiologists joined the group. Adoption of optimal culture methods (selective broth media and vaginorectal swabs) was strongly suggested by the group. GBS invasive diseases, which occurred during 2003–2005 in 29 birth centers of Emilia-Romagna, were prospectively collected. Incidence, RFs, and clinical features were analyzed to know the current burden of disease after having followed preventive strategies.

	METHODS

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Study Design
The aim of the study was to obtain data on culture-proven GBS infections observed in Emilia-Romagna. Public neonatal or pediatric departments were enrolled in a multicenter study during the last months of 2002. A network of 26 laboratories was created in 2003, and databases were searched for any additional cases of GBS-positive blood or cerebrospinal fluid culture. Periodical reminders about the study were sent to laboratories and to medical staff of each center every 2 months. Proven infections occurring between January 1, 2003, and December 31, 2005, in infants aged <90 days were prospectively recorded. Every subject notified by a source (ie, neonatal/pediatric departments or laboratories) was cross-checked with data obtained by the other source. Case subjects not confirmed by both sources were excluded.

Infant Sepsis Evaluation
A sepsis screen was obtained in neonates exhibiting signs of possible sepsis. Laboratory evaluation included at minimum a complete blood cell count with differential, C-reactive protein and a blood culture. If IAP was inadequate (<4 hours before delivery), healthy-appearing infants were screened. A lumbar puncture was not performed as part of the routine evaluation for sepsis in apparently healthy neonates. Ampicillin prophylaxis was administered (for 36–48 hours, pending cultures and laboratory results) to apparently healthy infants born to mothers with incomplete IAP, clinical RFs, and positive GBS status. Clinically ill newborn infants, infants born to mothers affected by chorioamnionitis, or infants born at a gestational age of <32 weeks received ampicillin and gentamicin until infection was excluded.

Definitions
Sepsis was defined as GBS bacteriemia in the presence of clinical signs and symptoms consistent with sepsis.¹³ Meningitis was diagnosed if GBS was recovered from cerebrospinal fluid in the presence of clinical signs of sepsis or if a positive blood-culture result was associated with cerebrospinal fluid pleocytosis and positive rapid test. Pneumonia was a respiratory distress syndrome with a radiographic appearance of streaky opacities or confluent lobar opacification that persisted for >24 hours in addition to a positive blood-culture result.¹⁴

Data Collection
Data on pregnancy, maternal screening cultures (vaginal or rectovaginal), presence of RFs, mode of delivery, agents used for chemoprophylaxis (IAP), dosing frequency, and timing relative to delivery were obtained for every proven infection. Neonatal clinical symptoms, age of onset, days of mechanical ventilation, therapies, and outcome were also recorded. If information obtained from charts was incomplete, each center was contacted by telephone to obtain missing details.

Microbiologic and Laboratory Methods
All 26 of the laboratories were contacted to obtain information on GBS culture techniques in use during 2003 (ie, transport media, incubation broth, and subculture on selective blood agar). The same investigation was repeated at the end of 2005. GBS serotyping started in 2005, after a collaborative study was undertaken with the World Health Organization Collaborating Centre of the Italian National Health Institute.

Statistical Methods
Statistical analysis was performed according to the nonparametric Mann-Whitney U test or the ² test. A P value of <.05 was used as the threshold for statistical significance and .10 < P < .05 as an indication of a trend for statistical significance. Data are presented as median ± 95% confidence interval.

	RESULTS

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There were 36255 live births in 2003, 37823 in 2004, and 38855 in 2005. Approximately 98.5% of infants were born in public birth centers. Preterm newborns comprised 7.4% of these births (data obtained from Regional Health Agency hospital discharge charts). All of the centers screened pregnant women who were at 35 to 37 weeks of gestation. Optimal culture methods were available from only 1 of 26 laboratories during 2003 but from 12 during 2005 (P = .001). Fifty-six cases of neonatal GBS infections were identified among 112933 live births, with an incidence of 0.50 per 1000 live births. The patient group included 35 male and 21 female infants. The incidence of disease is reported in Fig 1.

View larger version (14K): [in this window] [in a new window]   FIGURE 1 Incidence of EOD and LOD per 1000 live births during 2003–2005.

Twenty-six infants were born at term, and 4 were preterm (mean gestational age: 38.3 ± 0.6 weeks; range: 25–41 weeks). Eighteen mothers had no RFs, 8 had 1 RF only (there were 2 cases of ROM, 2 of maternal fever, 2 had preterm birth, and 2 had bacteriuria). Four mothers had 2 RFs: prematurity and ROM (1 case); fever and ROM (2 cases); and prematurity, ROM, and bacteriuria (1 case). Information on bacteriuria during pregnancy was not available for 6 cases.

Maternal cultures, obtained in the last 5 weeks before delivery, were available for 21 of 26 term infants and for 1 of 4 preterm infants. Data on maternal GBS status, RFs, and prophylaxis are shown in Table 1. Among 17 screened negative mothers, 5 had 1 RF; 5 mothers had vaginorectal swab, but culture methods were optimal in only 1 of 17 subjects.

Eleven of 30 infants either apparently had no signs (7 cases) or were mildly ill, that is, unexplained jaundice (2 cases), transient grunting (1 case), or mild gastric bleeding (1 case). Asymptomatic infants underwent blood cultures because of clinical RFs or positive maternal GBS status. Three infants of 7 who had no symptoms did not receive antibiotics and later were persistently healthy.

Nineteen showed moderate-to-severe symptoms; among them, 7 were ill at birth, and 16 of 19 were ill within 12 hours. Two preterm newborn infants presented with septic shock at birth and died within a few hours. Thirteen had respiratory symptoms as the predominant sign at the onset. Clinical findings, days of mechanical ventilation, and rate of severe brain sequelae at discharge are shown in Table 2. Meningitis was rare, but a considerable number of infants (21 of 30 infants) did not undergo a lumbar puncture.

Among 26 infants, 3 were mildly ill (mild fever only), and 23 had moderate-to-severe disease. In 15 subjects, symptoms started between 10 and 30 days of life and in 9 subjects between 31 and 60 days. Fever was the predominant sign at the onset (15 subjects). Meningitis was very common among 15 infants who had a lumbar puncture. Three infants completed IAP (by wide-spectrum antibiotics), and 4 were treated during the first days of life for GBS prevention. Four infants died because of overwhelming late-onset sepsis; 3 of them were preterm and had been treated in the perinatal period. Clinical findings, days of mechanical ventilation, and rate of severe brain sequelae at discharge are shown in Table 2.

Comparison Between EOD and LOD
There were no differences between EOD and LOD with respect to mean gestational age, mean Apgar score at minute 5, gender, vaginal delivery, maternal colonization, or RF, whereas a trend for a significant effect was observed for a lower birth weight among LOD (3206 ± 129 g [EOD] vs 2812 ± 197 g [LOD]; P = .084). A comparison between EODs and LODs is reported in Table 2. Infants who were asymptomatic or mildly ill (P = .063) were more common among EODs, as were infants with respiratory symptoms at presentation. In contrast, infants with meningitis (P = .019) or fever at presentation (P < .001) were significantly more frequent among LODs. Also, the number of preterm births, mortality rate, and the number of ventilated infants and severe brain sequelae at discharge were higher (even if not significantly) among LODs. Finally, the age of onset of disease did not show any difference between infants with EOD or LOD regardless of whether they had received prophylaxis (Table 3).

	DISCUSSION

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We investigated an area in which a screening-based approach has been implemented, obtaining the first baseline Italian population data. A significant rate of morbidity and mortality was found in infants who suffered from disease.

The analysis of persisting EOD cases showed several faults in the screening approach. Some cases occurred because of unavailability of pertinent patient data at delivery and some for time limitations to complete prophylaxis or for ineffectiveness of antimicrobial agents. Finally, most mothers of infants with EOD (17 of 22) were screened GBS-negative, but cultures were appropriate only for 1 of 30 cases. False-negative results may be the consequence of inconsistent policies for prevention (ie, use of cervical or vaginal rather rectovaginal sampling or culture on nonselective broth media). Pinto et al¹⁵ found that, of 92 mothers of infants with EOD, 22 had been GBS screened. Eighteen of 22 were culture-negative because of suboptimal culture techniques or because maternal swabs were collected >6 weeks before delivery. However, EOD may occur in infants born to GBS-negative women even if screening is appropriate.^{15, 16} In a retrospective analysis of 25 EODs, Puopolo et al¹⁷ found that 14 of 17 mothers of term infants affected by disease did not receive prophylaxis because they were screened negative for GBS. Recently it has been observed that the rate of maternal GBS carriage could be considerably higher than that predicted by late antenatal cultures. Repeated detection after pregnancy of the same GBS clone in women who were recorded as intermittent carriers suggests that fluctuations in the GBS proportions of the vaginorectal flora may occasionally preclude the detection of colonization.¹⁸ Finally, in a clinical setting, a multitude of factors, often unverifiable (ie, inappropriate sites of maternal sampling, improper swab storage, or transfer practice), may determine misleading screening results and contribute to the persistence of disease.

In our region, LODs were more severe than EODs, because more newborn infants were critically ill, received mechanical ventilation, or died. The higher severity of LODs found in the present study remains unclear, but the seriousness of EOD could have been minimized by an earlier diagnosis. The attention given by clinicians to infants at risk during the first hours of life could explain this finding.

Meningitis was very common among infants with LOD who underwent a lumbar puncture. This aspect is worth some attention, because residual disabilities at age 5 years have been reported in up to half of the cases of GBS meningitis.¹⁹

Five of 6 infants who died because of GBS infection were born premature, and 4 were affected by LOD. Interestingly, perinatal wide-spectrum antibiotics did not prevent the onset of a severe disease some weeks after. A low placental transfer of maternal immunoglobulin G antibodies, together with immunologic immaturity of premature infants, may predispose to disease. Unlike earlier studies, in recent years, preterm infants have been suffering mostly from LOD rather than EOD.^{7, 20} We believe that this change of disease rises mostly from preventive strategies, because the widespread use of IAP for preterm labor reduces the yield of GBS in cultures at birth. Unpublished data, which we obtained recently from some regional hospitals, showed that a high rate of women at risk (25%–35% of parturient) received IAP during the study period. In addition, we cannot exclude that some preterm infants had received antibiotics at birth before the collection of systemic cultures.

We found a rate of EOD incidence (0.27 per 1000 live births) that is considerably lower than the rate reported in most European countries and in previous smaller Italian studies. This is apparently not correlated with a lower maternal GBS carriage, because recent data obtained from hospitals where optimal culture methods are in use (A.B., L.L., K.R., et al, unpublished data, 2005–2006) suggest that rectovaginal carriage of pregnant women in Emilia-Romagna is high (18%–39%) and is comparable to that in the United States (15%–30%).²

Preventive strategies reduce the rate of the disease. Indeed, following a screening approach, a decrease in EOD incidence (from 1.45 to 0.45 per 1000 live births) was observed in a Spanish hospital network.²¹ We cannot demonstrate that a low rate of EOD incidence in Emilia-Romagna is a result of our policies, because there are no consistent Italian data on GBS disease in the era before prophylaxis. However, EOD incidence is comparable to that reported recently by Fluegge et al²⁰ in Germany (0.28 per 1000 live births), where a strategy that combines the risk and screening approach is in place.

Information about LOD is very scant in Europe, and no studies have investigated changes after the adoption of IAP. It is difficult to compare data from different countries, because definitions of disease and data sources differ among studies. However, LODs in most reports are 2 to 8 times less common than EODs and range from 0.07 to 0.25 per 1000 live births.^22–27 In Emilia-Romagna, the rate of LOD incidence was 0.23 per 1000 live births with an insignificant increase observed during 2005. This worrisome trend was confirmed by preliminary data from the first 10 months of 2006 (7 cases of EOD and 17 cases of LOD). It is interesting to note that the same trend has been reported in the US surveys, where a screening approach is adopted. LODs did not decrease as EODs, and late diseases are now more than half of reported infections.⁷

The hypothesis that IAP delays the onset of LOD is not supported by our data. However, because of the small number of cases, additional investigations are needed to address this issue.

Our study has some limits. Much data suggest that GBS invasive diseases are more common than found. First, the true incidence of EOD could be higher, because of low sensitivity of systemic cultures, ²⁸ particularly after IAP. This effect could be relevant, because a high rate of women at risk during the study period received prophylaxis, as reported above.

The number of infections may be underestimated by >20% if we consider only the cases reported by clinicians or microbiologists.²⁶ In addition, it may be possible that some newborns may have received an incomplete investigation, being empirically treated without the collection of systemic cultures, as reported elsewhere.^{12, 20, 29} It should be noted that the burden of this bias has not been investigated and may partly explain a lower rate of disease in some studies.

Finally, most newborns in our study, mainly those affected by EOD, did not undergo a lumbar puncture; as a result, the number of central nervous system infections may have been underestimated. Meningitis may occur even if blood cultures are negative or may complicate early infections, because it is clinically indistinguishable from bacteriemia without a focus.¹ However, even if the number of cases is small, early meningitis was fairly uncommon among infants who underwent a lumbar puncture. The rate that we found (22.2%) is comparable to that reported in Germany (16.0%).²⁰

	CONCLUSIONS

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The total rate of GBS neonatal infections in our region is low, but LODs are more severe than EODs, and prognosis is worthwhile. It will be difficult to prevent late infections, because maternal prophylaxis and neonatal antibiotic therapy at birth have no effect. This goal could only be achieved when active immunization becomes available. An approach that combines the mother's vaccination with other preventive measures at birth could be the best option. We believe that the aim of future strategies should be in the prevention of all GBS invasive diseases.

	ACKNOWLEDGMENTS

 
We thank Dr Mauro Stronati, who gave critical suggestions and revised the manuscript.

	FOOTNOTES

 
Accepted Feb 20, 2007.

Address correspondence to Alberto Berardi, MD, Dipartimento Materno-Infantile, Unità Operativa di Assistenza Neonatale, Università di Modena e Reggio Emilia, Via del Pozzo, 71-41100 Modena, Italy. E-mail: berardi.alberto{at}policlinico.mo.it

The authors have indicated they have no financial relationships relevant to this article to disclose.

	REFERENCES

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This article has been cited by other articles:

				A Berardi, L Lugli, C Rossi, M S Morini, F Vagnarelli, and F Ferrari Group B streptococcus and preventive strategies in Europe Arch. Dis. Child. Fetal Neonatal Ed., May 1, 2008; 93(3): F249 - F249. [Full Text] [PDF]

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