Strategies to Decrease Pertussis Transmission to Infants Kevin Forsyth, MD, PhDa, Stanley Plotkin, MDb, Tina Tan, MDc, Carl Heinz Wirsing von König, MDd

The Global Pertussis Initiative (GPI) is an expert scientific forum addressing abstract the worldwide burden of pertussis, which remains a serious health issue, especially in infants. This age cohort is at risk for developing pertussis by transmission from those in close proximity. Risk is increased in infants aged 0 to 6 weeks, as they are too young to be vaccinated. Older infants are at risk when their schedules are incomplete. Infants also bear the greatest disease burden owing to their high risk for pertussis-related complications and death; therefore, protecting them is a high priority. Two strategies have been proposed to protect infants. The first involves vaccinating pregnant women, which directly protects through the passive transfer of pertussis antibodies. The second strategy, cocooning, involves vaccinating parents, caregivers, and other close contacts, which indirectly protects infants from transmission by preventing disease in those in close proximity. The goal of this review was to present and discuss evidence on these 2 strategies. Based on available data, the GPI recommends vaccination during pregnancy as the primary strategy, given its efficacy, safety, and logistic advantages over a cocoon approach. If vaccination during pregnancy is not feasible, then all individuals having close contact with infants ,6 months old should be immunized consistent with local health authority guidelines. These efforts are anticipated to minimize pertussis transmission to vulnerable infants, although real-world effectiveness data are limited. Countries should educate lay and medical communities on pertussis and introduce robust surveillance practices while implementing these protective strategies.

aDepartment of Paediatrics and Child Health, Flinders Medical Centre, Flinders University, Adelaide, Australia; bDepartment of Pediatrics, University of Pennsylvania, c BRIEF OVERVIEW OF RECENT PERTUSSIS Philadelphia, Pennsylvania; Northwestern University, is waning , which has been Feinberg School of Medicine, Chicago, Illinois; and dLabor; observed despite vaccination. Medizin Krefeld MVZ, Krefeld, Germany

Pertussis () is caused Infants, especially those aged 0 to All authors participated in the review of the by the bacteria Bordetella pertussis 6 months, are at particular risk of literature, the formulation of the recommendations, transmitted through aerosol droplets. developing pertussis via transmission and the writing of the paper and approved the final manuscript as submitted. Although whole-cell and acellular from those in close proximity. Those vaccine formulations against aged 0 to 6 weeks are too young to be www.pediatrics.org/cgi/doi/10.1542/peds.2014-3925 B pertussis are available and coverage vaccinated against the disease, since DOI: 10.1542/peds.2014-3925 is high in most regions worldwide, infant schedules begin at 6 weeks and Accepted for publication Mar 13, 2015 pertussis remains a global health later depending on the country. Older Address correspondence to Kevin Forsyth, MD, PhD, 1 problem in almost all age groups. infants are at risk if they have not Professor of Paediatrics, Flinders University, Many countries with long histories of completed the pertussis vaccination Adelaide, Australia 5042. E-mail: kevin.forsyth@ routine pertussis vaccination have schedule series. Typically, the first flinders.edu.au experienced a recent resurgence of the is administered at PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, disease, particularly among older age 6 or 8 weeks, but it can be 1098-4275). children, adolescents, and adults. One administered as late as 3 months in Copyright © 2015 by the American Academy of factor that may be contributing to this some countries. This first dose Pediatrics

Downloaded from www.aappublications.org/news by guest on October 2, 2021 PEDIATRICS Volume 135, number 6, June 2015 SPECIAL ARTICLE produces partial protection mainly strategies to reduce the disease Practices (ACIP) of the against severe disease; higher rates of burden in infants, and prevent the Centers for Disease Control and immunity (80%– 90%) do not occur waning of immunity in older children Prevention (CDC) in 2011 until after administration of the third and adolescents. To achieve these recommended a pregnancy booster,10 dose.2–5 goals, GPI convenes global and and similar recommendations were In addition to being at increased risk regional meetings, attended by adopted to protect newborns in fi for developing pertussis, infants also experts from specialized elds, who Argentina, Belgium, Israel, New bear the greatest disease burden: work together to achieve a consensus Zealand, and the United 11,12 they have the highest risk for on recommendations for Kingdom. In the United pertussis-related complications and immunization strategies that will be Kingdom, in 2011, a steep increase death because they are more acceptable at local, national, and in pertussis activity occurred that susceptible to severe and fatal regional levels. Immunization disproportionately affected infants, disease. A recent surveillance study of strategies that focus on preventing and in response to this resurgence, in B pertussis patients hospitalized with pertussis transmission of to infants, 2012, the British Department of revealed that the hospitalization rate who can be unvaccinated or Health recommended that all women, for infants ,12 months old was underprotected, have been a focal during each pregnancy, be vaccinated notably higher at 38.8 per 100 000 point of the most recent GPI meetings against pertussis between 28 ’ 11 population than the rate in patients and published papers. Two such and 38 weeks gestation. Also fi younger than 16 years, which was 2.6 strategies are maternal immunization in 2012, the ACIP modi ed its per 100 000.6 In infants, increased during pregnancy, which directly recommendation to advocate 13 vulnerability was also observed protects the infant through the vaccination during each pregnancy, during the 2010 and 2012 outbreaks. passive transfer of antibodies from on the basis of evidence that antibody fi During the 2010 outbreak in mother to fetus, and cocooning, which levels decline signi cantly 1 year 14,15 California, 9477 individuals were indirectly protects infants through the postimmunization. In addition, diagnosed with pertussis, and vaccination of individuals who are in 2 years postvaccination, antibody although all age cohorts were close contact with them and are often levels measured from cord blood affected, the highest rates of disease the source of . This paper were found to be too low to provide 16 and hospitalization occurred in reviews and discusses empirical protection in infants. Thus, to infants ,6 months old.7 Similarly, in evidence related to both strategies optimize the concentration of 2012, outbreaks occurred in several and proposes public policy antibodies transferred to the neonate US states and a total of 48 277 cases recommendations to help protect near birth, ACIP now recommends were reported, with the highest infants from the risk of developing that vaccination occur during the 16 incidence rates occurring in infants pertussis. third trimester. Of note, 1 study ,1 year old.8 In the UK, a notable found that the active transport of increase in pertussis activity occurred maternal immunoglobulin G does not VACCINATION AGAINST PERTUSSIS ’ in 2011 through 2012.9 During that substantially occur before 30 weeks DURING PREGNANCY 17 time, the highest incidence occurred gestation. in infants ,3 months old, but Vaccination Recommendations and a notable increase also occurred in Uptake Transfer of the Maternal Pertussis the age cohort of $15 years. In There is strong evidence that the Antibodies After Vaccination addition, during those outbreaks the pregnancy booster directly protects To date, several studies have majority of deaths occurred in infants young infants through the transfer of confirmed that pertussis antibodies ,3 months old. Thus, when maternal pertussis antibodies, in are transferred from mother to fetus considering prevention strategies addition to being effective, safe, and after vaccination or natural against pertussis, it is critical to well tolerated. A key benefit of this infection.18–24 Only 1 randomized, include approaches that prevent approach is that it provides double-blind, placebo-controlled pertussis transmission to young protection to the very young from assessed maternal infants. birth until infant-generated immunity antibody transfer in infants born to is achieved from the primary women vaccinated during series of pertussis immunization. pregnancy.22 This phase 1–2, National GPI Vaccination during pregnancy is Institutes of Health–funded trial GPI was initiated in 2001 to now recommended by the national found that vaccination in the third raise global awareness about health organizations of several trimester produced a higher pertussis, develop evidence-based countries. In the United States, concentration of pertussis antibodies recommendations for vaccination the Advisory Committee on in infants at birth and age 2 months,

Downloaded from www.aappublications.org/news by guest on October 2, 2021 e1476 FORSYTH et al compared with infants of women who the number of reported cases peaking infection. By contrast, low VE (38%) received placebo. Transplacental in October. During this outbreak, resulted when immunization antibody transfer has been confirmed infants, especially those ,3 months occurred late in pregnancy, when it in other studies, which similarly old, were disproportionally would be expected that minimal found significantly higher antibody affected.11,25 Laboratory-confirmed antibodies would be transferred and titers in the infants of women cases between January 2008 and mothers might still be susceptible to vaccinated before or during September 2013 were extracted from infection. Although much remains pregnancy.18,19 Finally, 1 study has a national reference. Maternal vaccine unknown due to the limited data observed higher pertussis antibody effectiveness (VE) and coverage were available, the results from this study levels in infants at birth, presumably calculated based on 26 684 women suggest the likelihood that observed due to natural maternal infection.20 with a live birth from October 1, transfer of maternal pertussis Uptake of the pregnancy booster has 2012, to September 3, 2012, and antibodies after the pregnancy been assessed in the United Kingdom across that time period, overall booster confers some protection in 22 and the United States after the formal coverage was 64%, peaking at 78% very young infants. recommendations. Although universal during the beginning of 2013. A second more recent study also adoption has lagged greatly in both Consistent with the rise in maternal analyzed data from the United fi countries, uptake in the United coverage, the number of con rmed Kingdom after implementation of the , Kingdom was higher overall: ∼64% of cases in infants 3 months old pregnancy booster program. This fi pregnant women were vaccinated during the rst 9 months of 2013 was case-controlled study was designed to 9 months postrecommendation.25,26 lower compared with the same period estimate VE for protecting infants In contrast, 2 years after the US in 2012 (328 cases in 2012 vs 72 against pertussis by analyzing data recommendation, a comparison cases in 2013; 78% decrease; 95% collected between October 2012 and across several studies finds great confidence interval [CI] –72 to –83). July 2013, after the recommendation variability in coverage, ranging from Of note, across the first 9 months of was made. Case infants ,8 weeks of 82% to as low as 14%.26–28 Adoption 2013, all age groups experienced age with laboratory-confirmed is likely influenced by physician a decrease in the number of pertussis were identified in a national attitudes, parental opinions, and confirmed cases, but the decrease in reference laboratory, and healthy logistics, among other factors. One infants ,3 months old was controls were obtained from the logistic factor that might contribute to proportionately the greatest. In pediatric practices of each case infant. the greater uptake in the United addition, a comparison of reported The results found that significantly Kingdom is that pregnant women cases between 2013 and 2011 found more mothers (71%) of the controls receive their care from general that infants ,3 months old were the were vaccinated against pertussis practitioners, who are responsible for only age cohort that had fewer cases during pregnancy compared with the administering all across in 2013 (73) compared with 2011 case mothers (17%). The unadjusted all patients.26 In the United States, (118), consistent with the VE was 91% (95% CI 77% to 97%), pregnant women are seen by effectiveness of vaccination against confirming that vaccination against obstetricians, who are less likely to pertussis during pregnancy. A pertussis during pregnancy was routinely vaccinate patients.26 To decrease in pertussis-related effective at reducing disease in date, there have been no assessments hospitalizations was also newborns. of vaccine coverage in pregnant proportionately greater in infants ,3 women in developing countries. months old during the first 9 months Safety of the Pertussis Vaccine of 2013 compared with the same time During Pregnancy fi Clinical Bene ts Associated With period in 2012 (440 in 2012 vs 140 An established record of safety is Vaccination During Pregnancy in 2013; 68% decrease; 95% CI –61 critical for recommending that all The first evidence demonstrating the to –74). VE for vaccination $7days women receive the booster during effectiveness of vaccination during before birth in infants ,3 months old pregnancy. To date, the research finds pregnancy for the prevention of was 91% (95% CI 84% to 95%). VE that vaccination against pertussis infant disease comes from a study was affected by the timing of during pregnancy is well tolerated conducted in the United Kingdom vaccination during pregnancy and and not associated with any safety that compared data before and after was greatest (91%) when it occurred outcomes. Only 1 randomized, implementation of a pregnancy $28 days before birth, presumably double-blind, placebo-controlled booster program in 2012. This owing to an optimal quantity of clinical trial assessed safety in infants program was created in response to antibodies being transferred to the born to pregnant women who a significant outbreak that began in neonate18–20,22–24,29; this timing also received the vaccine.22 In this study, 2011 and extended into 2012, with eliminates the mothers as a source of maternal and infant adverse events

Downloaded from www.aappublications.org/news by guest on October 2, 2021 PEDIATRICS Volume 135, number 6, June 2015 e1477 and infant growth and development that a diagnosis of chorioamnionitis infants.36 Many studies have until age 13 months were evaluated. had only a 50% positive predictive confirmed that the majority of infants No adverse events were observed and value for clinical symptoms with pertussis were infected by there were no differences in infant consistent with the outcome. In total, a relative with whom they came into growth and development. the results from all these studies close contact.6,37–39 Parents, The safety of pertussis vaccination provide initial evidence that especially mothers, have been fi during pregnancy was also evaluated vaccination against pertussis during identi ed as the primary source . in 2 retrospective, observational pregnancy is well tolerated and is not ( 50%) of transmission because they studies conducted in the United associated with an increased risk of spend the most time with their Kingdom and the United States.30,31 adverse events. infants. The cocoon strategy involves The goal of both was to determine One possible safety issue that has vaccinating those in close proximity whether immunization was been raised is whether antibodies to infants, which indirectly protects associated with an increased risk produced from pertussis vaccination them from transmission by of adverse obstetric events or during pregnancy will interfere with preventing disease in parents, family adverse birth or neonatal outcomes. protection during the infant schedule, members, and other caregivers. Vaccinated pregnant women were an outcome referred to as “blunting.” Cocooning is rational from an identified within 2 large databases Three studies, including 1 immunologic perspective, as the (US: California Vaccine Safety randomized clinical trial, found that kinetics of the humoral response after Datalink; UK: Clinical Practice the immune response in infants after Tdap immunization is rapid, with Research Datalink), resulting in an acellular vaccine was not affected 88% to 94% of vaccinated individuals a cohort of 46 305 women who were by neonatal antibodies generated by developing maximal antibody titers 40,41 then compared with matched maternal immunization, whereas within 2 weeks. However, unvaccinated controls. The adverse blunting resulted after a whole-cell because immunity is not immediate, if birth or neonate outcomes included vaccine.20,22,32,33 vaccination occurs solely during the preterm or small for gestational age postpartum period, there will be # birth, low birth weight, fetal distress, Challenges to Implementing a short time ( 2 weeks neonatal renal failure, and stillbirth. Vaccination During Pregnancy postvaccination) when the infant could be at risk for transmission.40,41 The adverse obstetric events included Several challenges related to maternal hypertensive disorders, vaccination during pregnancy have fi chorioamnionitis, maternal death, been identified, including lack of Clinical Bene ts Associated With Cocooning antepartum and postpartum perceived benefit by pregnant hemorrhage, uterine rupture, women, cost, lack of transportation, The effectiveness of the cocoon placenta previa, vasa previa, and work commitments, and fear of strategy on pertussis-related cesarean delivery. No increased risk needles.34 However, studies have outcomes has been evaluated in 2 of adverse birth or neonatal outcomes highlighted that recommendations of small studies to date.42 The first was observed. In addition, no healthcare providers (HCPs) are key found that postpartum vaccination increased risk of adverse obstetric to vaccine uptake, as is educating targeting only mothers was not events was found with the exception pregnant women on the benefits of associated with a decrease in the of a small but statistically significant immunization for the young number of pertussis cases.42 The increased risk of chorioamnionitis infant.34,35 In 1 survey-based study, authors concluded that extending diagnosis (6.1% vs 5.5% [adjusted although the majority of women vaccination to all individuals who are relative risk estimate, 1.19; 95% CI (80%) reported willingness to be in close contact with newborns may 1.13 to 1.26]). However, given that vaccinated against pertussis during be more effective. In contrast, a more the magnitude of risk was small, the pregnancy should it be recent case-control study conducted authors stress that this finding should recommended, 45% had never heard to assess the effectiveness of be interpreted with caution, of the vaccine, had never thought a government-funded cocoon especially since the study observed about it, or were undecided about program found the vaccination no associated increased risk of having it.35 strategy to be effective at preventing preterm birth, which is a major disease in young infants.43 The sequela of chorioamnionitis. An program was implemented during alternative explanation for the THE COCOON VACCINATION STRATEGY a pertussis epidemic in Australia. In increased chorioamnionitis risk is Waning immunity has been observed the study, laboratory-confirmed that it reflects differences in diagnosis in children, adolescents, and adults, pertussis cases occurring in young across the subjects in the study, as and these cohorts serve as sources of infants ,4 months old were a review of the medical records found infection for underprotected identified and then the parental

Downloaded from www.aappublications.org/news by guest on October 2, 2021 e1478 FORSYTH et al reported vaccination status was ascertained. Cocooning was defined as vaccination occurring $4 weeks before the case symptom onset in the young infants. The results found that the mothers of infants diagnosed with pertussis were less likely to have been immunized (22% vs 32%), as were the fathers (20% vs 31%). Parental cocooning was found to decrease the risk of pertussis by 51% in the infants. The effectiveness of cocooning on pertussis-related outcomes has also been evaluated using computer simulations and statistical analyses. Several studies (from Canada, Italy, and the United States) have estimated effectiveness by calculating the FIGURE 1 number needed to vaccinate to GPI recommendations to avoid newborn and infant pertussis deaths and severe disease. Protection prevent pertussis outcomes.44–46 by cocooning depends on vaccinating all who come in contact with the infant. About 2 weeks are required for antibodies to develop in vaccinated contacts. Three of the analyses suggested that under the conditions of low pertussis incidence, the cocoon strategy is not estimated that cocooning would be length of hospital stay affected fi ef cient and would be very resource- more expensive to implement than cocooning implementation, as the intensive owing to the large numbers other strategies designed to protect shorter the infant’s stay, the less likely of individuals who would need to be infants from pertussis. it was that the family would be vaccinated to prevent disease-related vaccinated.53 These studies found 44–46 outcomes. In contrast, a fourth Challenges to Implementing that vaccine uptake was greatest in study that compared various Cocooning mothers (75%–86%)41 compared vaccination strategies found that the For cocooning to successfully prevent with fathers (58%), aunts (19%), or cocooning of parents of newborns grandparents (12%).50 paired with an adult booster would pertussis transmission to newborns, maintain a low level of pertussis several challenges arise based on the Acceptance of cocooning can also be need to vaccinate multiple increased when both family members incidence while being the most cost- individuals. First, this strategy can be and HCPs perceive a benefit to the effective approach over a wide range very costly and resource-intensive to newborn from cocooning. This was of scenarios.47 These strategies implement, in terms of securing not highlighted by a recent educational included combinations of the infant only adequate staff but also program implemented in an Italian primary series, adolescent booster, reimbursement or alternative funding hospital.54 Initially, a free postpartum cocooning, and adult booster. for the .41 A second key DTaP was offered to The cost-effectiveness of cocooning challenge to implementing cocooning parents and household contacts, but has also been analyzed. Using is acceptance by the newborn’s family only 3% of the invited families dynamic population effects, and close contacts. Vaccination participated. To increase uptake, an cocooning has been found to reduce uptake can be increased in family educational program was introduced, the costs associated with pertussis.48 members and close contacts by HCPs were recruited and engaged, Similarly, another model, using improving logistics. For example, and interactions with the families a base-case analysis, estimated that several studies found that most were increased during visiting hours. cocooning would be cost-effective family members are receptive to These approaches proved successful, from both a payer and societal being immunized against pertussis if and by the end of the pilot program, perspective, as it was associated with the vaccination is made easily 79% of the new mothers were the highest number of quality- accessible (eg, during routine vaccinated. Consistent with this, adjusted life-years gained (although hospital, clinic, or office visits).41,50–52 another study found that although this observation was mostly in Consistent with this, 1 study in many new parents’ knowledge about adults).49 However, this model a neonatal ICU determined that pertussis was scarce, many (mothers:

Downloaded from www.aappublications.org/news by guest on October 2, 2021 PEDIATRICS Volume 135, number 6, June 2015 e1479 64%; fathers: 59%) accepted A Comparison of the Cost- strategy (Fig 1). If maternal vaccination if it was recommended by Effectiveness of Maternal immunization is not possible, or if a healthcare provider .55 Immunization Versus Cocooning families desire additional protective Additional challenges to consider The cost-effectiveness of the 2 measures for their newborns, then it is when implementing cocooning vaccination strategies has been recommended that all individuals , include changes in disease compared using mathematical having close contact with infants 6 epidemiology and geographic modeling. One study, using a Markov months old be immunized consistent differences in child-rearing practices, cohort model, found that the pregnancy with local health authority guidelines. A both of which will affect how the booster was projected to be more high priority should be given to fi strategy should be adapted to meet cost-effective, and also associated with achieving a complete cocoon, de ned local needs. For example, complete a reduction in pertussis-related as full immunization of the family, since cocooning was successfully outcomes in infants.56 The pregnancy the robustness of protection against implemented (76% of families booster could attenuate the number of pertussis is a function of the number of with newborns) in a hospital-based cases by 33% (vs 20% for cocooning), infant contacts vaccinated. If vaccine clinic during a 2010 hospitalizations by 38% (vs 19%), a complete cocoon is not possible, then pertussis outbreak.51 In contrast, and deaths by 49% (vs 16%). Of note, the next priority is vaccination of both during 2 control (nonoutbreak) the model found that postpartum parents, followed by the mother only periods, only 29% of the families vaccination of the father plus 1 (Fig 1). For families using cocooning, achieved a complete cocoon. Local grandparent would decrease the immunization should occur during the sociologic factors also need to be number of cases by an additional pregnancy or immediately postpartum considered if cocooning is to be 16%,butatahighercost.Vaccination to prevent pertussis transmission to implemented successfully, and high during pregnancy produced a cost per infants ,6monthsold.Itisimportant adherence rates are to be ensured. quality-adjusted life-year that was to note, however, that real-world data For example, in some geographic considerably less ($414 523 vs $1 172 remain limited on the clinical regions, family units may consist 825) than cocooning. effectiveness of vaccination against of a small number of individuals, the pertussis during pregnancy and of parents only, or a small number of cocooning, especially in the form of siblings. In other areas, extended GPI RECOMMENDATIONS large clinical trials. As we expect future families are more common, Based on available evidence, the GPI studies will yield new data, these will necessitating the targeting of much recommends maternal immunization be incorporated into future wider groups. during pregnancy as the primary recommendations.

FINANCIAL DISCLOSURE: Dr Forsyth has received honoraria from Sanofi Pasteur. Dr Plotkin is a paid consultant to Sanofi Pasteur, Merck & Co., and GlaxoSmithKline Biologicals. Dr Tan has received grants from Merck & Co. and Sanofi Pasteur and personal fees from GlaxoSmithKline Biologicals and Sanofi Pasteur. Dr Wirsing von Kӧnig has received honoraria for attending meetings sponsored by Sanofi Pasteur, GlaxoSmithKline Biologicals SA, and Novartis Vaccines. FUNDING: Medical writing support was provided by Shelley Lindley, PhD, and Mary Burder, PhD, of PAREXEL, which was funded by Sanofi Pasteur. The Global Pertussis Initiative (GPI) is supported by Sanofi Pasteur SA and was established in 2001 to evaluate the ongoing problem of pertussis worldwide and to recommend appropriate pertussis control strategies. Sanofi Pasteur continues to fund this important initiative to provide a forum for scientific and policy-based discussions. The views and opinions expressed in this publication, which could include use of Sanofi Pasteur products that is inconsistent with current labeling or licensed indication, are solely those of the authors and do not reflect the position of Sanofi Pasteur SA. POTENTIAL CONFLICT OF INTEREST: Dr Forsyth has received honoraria from Sanofi Pasteur. Dr Plotkin is a paid consultant to Sanofi Pasteur, Merck & Co., and GlaxoSmithKline Biologicals. Dr Tan has received grants from Merck & Co. and Sanofi Pasteur and personal fees from GlaxoSmithKline Biologicals and Sanofi Pasteur. Dr Wirsing von Kӧnig has received honoraria for attending meetings sponsored by Sanofi Pasteur, GlaxoSmithKline Biologicals SA, and Novartis Vaccines. COMPANION PAPER: A companion to this article can be found on page e1483, online at www.pediatrics.org/cgi/doi/10.1542/peds.2015-0770.

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Downloaded from www.aappublications.org/news by guest on October 2, 2021 Strategies to Decrease Pertussis Transmission to Infants Kevin Forsyth, Stanley Plotkin, Tina Tan and Carl Heinz Wirsing von König Pediatrics 2015;135;e1475 DOI: 10.1542/peds.2014-3925 originally published online May 11, 2015;

The online version of this article, along with updated information and services, is located on the World Wide Web at: http://pediatrics.aappublications.org/content/135/6/e1475

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