Original Article. Thad R. Wilson, PhD, APRN, BC.

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1 Original Article Update on Adolescent Immunization: Review of Pertussis and the Efficacy, Safety, and Clinical Use of Vaccines That Contain Tetanus-Diphtheria- Acellular Pertussis Thad R. Wilson, PhD, APRN, BC ABSTRACT Adolescents, who comprise 14 of the US population, are historically resistant to receiving health care. As a result, adolescents have low immunization rates and are becoming more susceptible to diseases that are preventable by vaccine, such as pertussis. The incidence of pertussis has increased during the past 25 years, with a notable shift in incidence from young children to adolescents and young adults. Thad R. Wilson is Associate Dean for Academics, University of Missouri Kansas City School of Nursing, Kansas City, Mo. Reprint requests: Thad Wilson, PhD, APRN, BC, University of Missouri Kansas City School of Nursing, 2220 Holmes, HSB 101, Kansas City, MO 64108; wilsontr@umkc.edu /$32.00 Copyright 2006 by the National Association of Pediatric Nurse Practitioners. doi: /j.pedhc New vaccines that provide protection against pertussis for use in adolescents have been proven to be safe, effective, and cost-beneficial. Regional epidemics among infants and other vulnerable populations can be reduced or eliminated with improved immunity in adolescents. J Pediatr Health Care. (2006) 20, Fourteen percent of the current population of the United States is composed of adolescents between the ages of 10 and 19 years (US Census Bureau, 2000). Adolescents are generally considered a healthy group when compared with children and adults, but in reality, adolescents face unique health care challenges with rising rates of obesity, sexually transmitted infections, diabetes, violence, and substance abuse (Centers for Disease Control and Prevention [CDC], 2004c; Ozer, Park, Paul, Brindis, & Irwin, 2003). The Guidelines for Adolescent Preventive Services, developed by the American Medical Association s Department of Adolescent Health, recommend that adolescents annually schedule a routine visit with a health care provider (American Medical Association, 1997). Historically, it has been demonstrated that adolescents avoid using the health care system; for example, patients aged 11 to 21 years accounted for only 9.1 of total office visits in 1994 (Ziv, Boulet, & Slap, 1999). Yet in 2001, it was reported that 92 of adolescents had visited a provider during the previous year, although 68 of the visits were for acute illnesses or injuries (Foundation for Accountability, 2001). Primary care providers are more likely to vaccinate during a preventive health visit than during an illness-related visit or follow-up visit (Schaffer, Humiston, Shone, Averhoff, & Szilagyi, 2001), so adolescents may not be receiving currently recommended vaccines. Journal of Pediatric Health Care July/August

2 Determining adolescent immunization rates is challenging, but available data show that the rates have not met the Healthy People 2010 goal, which is to ensure that 90 of adolescents have received all recommended immunizations (US Department of Health and Human Services, 2000). Rickert et al. (2004) reported that in managed care organizations, 64 of adolescents had received two doses of measles-mumps-rubella vaccine (MMR) and only 38 had completed the three-dose hepatitis B vaccine (HepB) series. Similar results were reported from the National Health Interview Survey (MMR, 76; HepB, 55), which included tetanus and diphtheria vaccine (Td) coverage (76) (Dey & Bloom, 2005). The National Committee for Quality Assurance found similar rates (MMR, 72.6; HepB, 57.5) among persons with insurance, and even lower rates for persons with Medicaid (MMR, 67.9; HepB, 47.3) (National Committee for Quality Assurance, 2003). Greater challenges for adolescent vaccination lie ahead. The Institute of Medicine (2000) reported that five vaccines (cytomegalovirus, herpes simplex virus, human papillomavirus, parainfluenza, and respiratory syncytial virus) targeted to adolescents are likely to be in development in the near future. Providers, organizations, agencies, and the government may need to consider innovative strategies to help improve the delivery of vaccines to adolescents. Primary care providers should undertake adolescent vaccination strategies as intensely as they do infant vaccination. Two recently approved vaccines for adolescents contain tetanus toxoid, reduced diphtheria toxoid, and acellular pertussis () and protect against pertussis. Nurse practitioners need to be knowledgeable about pertussis and the vaccines used to prevent this disease in order to provide adequate protection for their patients. This article reviews the pathophysiology and epidemiology of pertussis and provides practical information about its prevention in adolescents using. OVERVIEW OF PERTUSSIS Pertussis is a highly communicable respiratory disease that generally is mild yet troublesome in adolescents but can be fatal in infants (CDC, 2005b). Transmission occurs primarily through respiratory secretions from infected persons. The initial symptoms lowgrade fever and mild cough have an insidious onset and last only 1 to 2 weeks in adolescents. Inspiratory whoop and cyanosis are uncommon in this age group, and the relatively short duration of symptoms often makes pertussis indistinguishable from other respiratory diseases. In infants, however, the cough often becomes more severe after 1 to 2 weeks (CDC, 2005b). These patients exhibit periods of numerous, rapid coughs (paroxysms), often accompanied by cyanosis and thick mucus expectoration. At the conclusion of each paroxysm, a high-pitched inspiration occurs, producing the characteristic whooping sound. Post-tussive vomiting also is common in Nurse practitioners need to be aware of the increasing incidence of pertussis in the United States and should consider pertussis in adolescents presenting with a cough. infants as well as adolescents (De Serres et al., 2000). Symptoms begin to dissipate after 2 to 3 weeks, but may persist for up to 3 months (CDC, 2005b). Because of its general nature and the similarity of its symptoms to other common respiratory illnesses, pertussis is difficult to diagnose in adolescents. Health care providers may incorrectly assume that fully vaccinated adolescents have another type of respiratory infection and direct their diagnosis away from pertussis. In one study, 54 of patients diagnosed with pertussis were initially misdiagnosed (Yaari et al., 1999). It is estimated that nationwide, only 12 of pertussis cases are actually reported and that underreporting may be most prevalent among adolescent and adult cases (Gürisuris et al., 1999). As a result, adolescents often are the source of pertussis infection for infants and young children (CDC, 2005b). One study of 255 individuals with household exposure to pertussis demonstrated that 90 of the index cases occurred in patients younger than 4 years (Deen et al., 1995). These index cases were traced to their corresponding primary cases, 53 of which occurred in patients at least Primary care providers should undertake adolescent vaccination strategies as intensely as they do infant vaccination. 230 Volume 20 Number 4 Journal of Pediatric Health Care

3 Cases, Thousands FIGURE 1. Reported cases of pertussis, United States, (From Centers for Disease Control and Prevention, 2005a, 2005c) Year FIGURE 2. Incidence and demographic shift of pertussis in the United States, (From Centers for Disease Massachusetts occurred in school settings (Yih et al., 2000). Incidence and Impact of Pertussis Pertussis is the only vaccine-preventable disease for which there has been a dramatic increase in its incidence in the United States during the past 25 years (Figure 1), and in 2004, 25,827 cases of pertussis were reported (CDC, 2005a, 2005c). In the past, the incidence of pertussis was highest in children from birth to age 4 years; however, the number of cases in the 5- to 14-year-old age group increased by 66 from 1993 to 1996 and another 62 from 1996 to 2003 (Figure 2) (CDC, 2005c, 2004a, 2001, 1997d, 1994). Notably, the number of pertussis cases in the 15- to 24- year-old age group increased sixfold. Among adults aged 25 years and older, the number of pertussis cases more than doubled between 1993 and 1996 and increased 332 from 1993 to Therefore, pertussis is likely underdiagnosed and underreported, and it has been estimated that more than 1 million Control and Prevention, 2005c, 2004a, 2001, 1997d, 1994). cases of pertussis occur yearly in persons older than 15 years (Strebel et al., 2001) It is unclear whether the recent rise in the incidence of pertussis is 2002 real or a reflection of improved diagnosis. In recent years, there has been a renewed emphasis on the occurrence of pertussis in the adolescent 2000 and young adult popula- tions. Recent publications in clinical 1500 journals have alerted providers to consider pertussis when evaluating 1000 patients who present with 500 cough (Dworkin, 2005; Hewlett & Edwards, 2005). Additionally, technologic 0 advances in the diagnosis <1 y 1-4 y 5-14 y y 25+ y of pertussis, such as polymerase chain reaction assay, have improved Age Group the likelihood of a pertus- sis diagnosis (CDC, 1997a). However, 13 years of age. These data were further substantiated by reports of outbreaks in which adolescents outbreaks in Massachusetts in 1992 indicated that 95 of pertussis cases occurred in adolescents aged since the 1980s, there has been an 11 increase in the incidence of pertussis among infants were the sources of infection 10 to 19 years. In 1996, 18 of 20 too young to receive three doses of (Davis, 2005). Reports of pertussis reported pertussis outbreaks in vaccine containing pertussis (CDC, Number of Cases Per Year Journal of Pediatric Health Care July/August

4 2002b). Because the incidence has increased in this well-recognized, high-risk group and others, it is unlikely that provider recognition or improved diagnostics are solely responsible for the observed rise in the incidence of pertussis. The number of pertussis cases among adolescents and young adults is alarming because individuals in these age groups should and can be protected adequately by vaccination. The first whole-cell pertussis vaccine was licensed in the late 1940s and contributed to a significant decline in the incidence of pertussis (CDC, 2002b). The disease reached a historic low in Following reports of high rates of local reactions such as redness, swelling, and pain at the injection site, mild systemic reactions such as fever, and possible association with more severe systemic reactions such as convulsions, hypotonic-hyporesponsive episodes, and acute encephalopathy, a more purified version, acellular pertussis vaccine, was introduced in 1991 (CDC, 2005b). Immunization rates for at least three doses of diphtheria, tetanus, and acellular pertussis vaccine (DTaP) among children entering school were 95 in 2003 (CDC, 2004b). Similar results for children 19 to 35 months of age were found in 1992 (83) and 1996 (95) (CDC, 1997c), indicating that immunization rates have been stable or increasing since at least Therefore, the increased incidence of pertussis in adolescents does not appear to correlate with poor vaccination coverage. An alternative explanation and the most widely accepted hypothesis is waning immunity following vaccination. Since the 1980s, there has been increasing evidence that the immunity gained through vaccination or natural infection with pertussis does not last a lifetime (Jenkinson, 1988). A 10-year study in England found that 5 years after vaccination, only 52 of those vaccinated maintained immunity. In the 1990s, several studies in Japan and the United States demonstrated that pertussis still developed in adolescents and adults who received the complete vaccination series (Aoyama, Arracima, Nishimura, & Saito, 1995; Cattaneo, Reed, Haase, Wills, & Edwards, 1996; CDC, 1997b; Kenyon et al., 1996; Khetsuriani et al., 2001). A 2003 outbreak in Wisconsin provided further evidence that immunity to pertussis wanes over time (Sotir et al., 2005). One alarming aspect of the increasing incidence of pertussis is that undiagnosed adolescents and adults can unknowingly expose susceptible individuals to this disease, including undervaccinated children and infants (Wirsing von König, Postels-Multani, Bock, & Schmitt, 1995). Health care providers not attuned to the possibility of pertussis in adolescents may not educate or warn families about the disease, allowing dangerous intrafamily and interfamily transmission (Aoyama et al., 1995; Kenyon et al., 1996). The growing incidence of pertussis is producing a significant economic burden on families and the health care system. It has been estimated that for an infant, the direct and indirect costs of a single case of pertussis can be more than $3500 (Pichichero & Treanor, 1997). Lee et al. (2004) found that on average, adolescents with pertussis miss 6 days of school, parents caring for their ill children miss 2 days of work, and adults with pertussis miss 10 days of work. They also found that the total cost of pertussis illness was $397 for each adolescent and $773 for each adult, and when the costs for treating contacts were included, the total cost was estimated at $804 and $1952 per case in adolescents and adults, respectively (Lee et al.). In addition, similar findings have been reported in other analyses (De Serres et al., 2000). PREVENTION WITH PERTUSSIS VACCINES The changing epidemiology of pertussis in the United States, particularly the shift of the disease burden from infants to adolescents and adults, has prompted the development and licensure of vaccines for use in this older age group. A vaccine has been used in Europe and Canada for universal vaccination of adolescents, and in a few countries in adults, for several years (Table 1) (Halperin, 2005; Wirsing von König et al., 1995). Recently, a vaccine, Boostrix (Glaxo- SmithKline Biologicals, Rixensart, Belgium), was approved in the United States for use in adolescents aged 10 through 18 years (Boostrix, 2005), and another, Adacel (Aventis Pasteur, Toronto, Canada), was approved for use in patients aged 11 to 64 years (Adacel, 2005). The antigenic components for the combination vaccines are provided in Table 2. The tetanus and diphtheria toxoids in these vaccines are similar to formulations of Td vaccines already licensed and commonly adminis- Although diagnosis of pertussis often is overlooked in adolescents presenting with cough illnesses, adolescents can be the source of pertussis infection for infants, a population in which disease can be severe. 232 Volume 20 Number 4 Journal of Pediatric Health Care

5 TABLE 1. Pertussis immunization schedules in countries reporting increased incidence of pertussis in adolescents and adults Country Previous schedule Revised schedule Product used Canada 4-6 y 4-6 y y France 2, 3, 4, mo 2, 3, 4, mo y Germany 2, 3, 4, mo 2, 3, 4, mo y Australia 2, 4, 6 mo 4y 4y y United States 4-6 y 4-6 y y* DTaP-IPV-Hib DTaP-IPV DTwP-IPV-Hib DTaP-IPV-Hib-HBV DTaP-HBV or DTaP DTaP DTaP or DTaP-IPV DTaP or DTaP-IPV DtaP, Diphtheria, tetanus, and acellular pertussis; DTwP, diphtheria, tetanus, and whole cell pertussis; HBV, hepatitis B virus; Hib, Haemophilus influenzae type b; IPV, injectable polio vaccine;, tetanus, diphtheria, and acellular pertussis. Adapted from Halperin, 2005, with permission, and the Advisory Committee on Immunization Practices, *Recommendation for adolescents aged 13 to 18 years not yet endorsed by the Centers for Disease Control and Prevention as of date of publication. TABLE 2. Comparison of tetanus toxoid, reduced diphtheria toxoid, and acellular pertussis () vaccines Antigenic component Boostrix Adacel PT ( g) FHA ( g) 8 5 PRN ( g) FIM 2 3( g) 5 D (Lf) T (Lf) 5 5 D, Diphtheria toxoid; FHA, filamentous hemagglutinin; FIM 2 3, fimbriae types 2 and 3; Lf,flocculation units; PRN, pertactin; PT, pertussis toxoid; T, tetanus toxoid. Data from Adacel, 2005, and Boostrix, tered to adolescents and adults in the United States (Broder & Mijalski, 2005). Both vaccines are administered in a single intramuscular dose of 0.5 ml (Adacel, 2005; Boostrix, 2005). Boostrix is available in prefilled syringes as well as vials. Clinical Effectiveness Using information from the National Immunization Survey (NIS) and surveillance data from 1998 to 1999, the CDC calculated that DTaP vaccines and whole-cell pertussis vaccine combined with diphtheria and tetanus toxoids (DTwP) administered during childhood are at least 88 effective (CDC, 2002b). However, the immunity induced by childhood vaccination or natural infection wanes after 5 to 13 years (CDC, 1997b; Cherry, 1999; Jenkinson, 1988; Le et al., 2004). Therefore, studies were conducted to determine if an acellular vaccine containing reduced quantities of pertussis antigens could adequately boost antibody response. A recent study conducted in the United States evaluated the immune response to one dose of or Td vaccine in 4114 adolescents aged 10 to 18 years (Friedland & Descamps, 2004). Investigators found that antibody response to the pertussis antigens pertussis toxin (PT) (geometric mean titer [GMT]: 85.9 EL U/mL), filamentous hemagglutinin (FHA) (GMT: EL U/mL), and pertactin (GMT: EL.U/mL) exceeded that observed in infants following primary immunization with DTaP. In a study in Finland of 510 healthy adolescents aged 10 to 13 years, all subjects who received a vaccine showed a significant rise (12- to 76-fold) in GMT of antibodies to tetanus and diphtheria toxoids and each of the pertussis antigens in the study vaccine (Minh et al., 1999). Similar results, which demonstrated a threefold to sixfold increase in GMT of pertussis antibodies, were reported in a study of 1583 adolescents in the In the past 25 years, the overall incidence of pertussis has increased, especially in adolescents and adults. This increase is thought to be the result of waning immunity to pertussis following vaccination. Journal of Pediatric Health Care July/August

6 TABLE 3. Percentage of subjects reporting adverse events following administration of vaccine Adverse event Pichichero et al., 2006 (n 3032) Pichichero et al., 2005 (n 2873) Halperin et al., 2000 (n 473) Van der Wielen et al., 2000 (n 96) Minh et al., 1999 (n 448) Pain at injection site Severe pain at injection site 4.6 NR 30.9* Headaches Severe headaches * Body ache NR NR NR Severe body ache NR NR 8.4* NR NR Fatigue Severe fatigue 3.7 NR 9.1* NR, Not reported. *Results reported as moderate reaction or more severe. United States (Daum, Marshall, Walter, & Bologa, 2004). In a study of 824 adults, 31.5 were seronegative for pertussis prior to administration of a vaccine containing pertussis (Van Damme & Burgess, 2004). One month after immunization, 93 were seropositive. A greater than eightfold increase in GMT of pertussis antibody was demonstrated 18 months after administration of the vaccine in another study involving 101 subjects (Le et al., 2004). Similar results were reported from a study of 746 adolescents and adults (Halperin et al., 2000). The majority (73 to 97) of adolescents or adults in the studies previously discussed also had levels of antibodies to the tetanus and diphtheria toxoids adequate for protection after administration of a booster dose of vaccine (Daum et al., 2004; Friedland & Descamps, 2004; Halperin et al., 2000; Le et al., 2004; Minh et al., 1999; Van Damme & Burgess, 2004). However, studies have not yet been undertaken to determine levels of pertussis antibody needed for protection in patients older than 18 years. In all studies, the GMT for antibodies against at least one of the pertussis antigens was greater than fourfold. Because similar antibody response in children younger than 6 years receiving the DTaP vaccine provides adequate protection, it is anticipated that the vaccine should provide adequate protection for adolescents and adults. Clinical Safety One of the main reasons adolescents have not been included in pertussis vaccination efforts during the past 30 years is because of the high rates of adverse reactions to whole-cell pertussis vaccines. However, acellular pertussis vaccines do not produce the same rates of adverse events and therefore have essentially replaced DTwP in clinical practice. Likewise, general adverse events following administration of have been infrequent and mild (Table 3). Adverse events reported for were similar in incidence and severity to those for Td (Halperin et al., 2000; Minh et al., 1999; Pichichero et al., 2006; Pichichero et al., 2005; Van der Wielen et al., 2000). Use of in Clinical Practice The Global Pertussis Initiative, an expert forum of the world s leading scientists, recommended establishment of universal adolescent immunization in countries that could afford to do so (Forsyth, et al., 2004). This recommendation is justified by years of increasing trends in the incidence of pertussis, particularly among adolescents and adults. The use of a safe and effective pertussis vaccine among adolescents is cost-effective, provided reasonable herd immunity would be gained (Purdy, Hay, Botteman, & Ward, 2004). Immunizing 80 of the adolescents in the United States would cost approximately $75 million but could prevent approximately 70,000 cases of The ACIP recommends replacing the current Td booster vaccine with vaccine in adolescents. is generally well tolerated and provides immunity to tetanus, diphtheria, and pertussis comparable to that produced by Td and DTaP vaccines. 234 Volume 20 Number 4 Journal of Pediatric Health Care

7 pertussis and 40 deaths yearly, saving $70 million (Caro et al., 2003). Nurse practitioners need to be aware of the increasing incidence of pertussis in the United States and should consider pertussis in adolescents presenting with a cough. Educating patients and parents on the severity and risk of contracting the disease with an emphasis on the role adolescents have in the transmission of pertussis, particularly to infants, is important. A discussion about the devastating outcomes for many infants infected by parents, siblings, and friends would be valuable, as would a discussion about the morbidity of pertussis in adolescents. Nurse practitioners should explain that the long duration of illness may cause adolescents to miss school and important life events, and that vaccination may prevent these consequences. Nurse practitioners also should reinforce the importance of vaccinating adolescents with vaccine by explaining that immunity to pertussis conferred by the last pertussis immunization (usually given at age 4 to 6 years) wanes over time. On June 30, 2005, the Advisory Committee on Immunization Practices (ACIP) (2005) recommended that health care providers administer vaccine in place of Td vaccine in adolescents 11 and 12 years of age. Adolescents aged 13 through 18 years who missed the dose of Td vaccine scheduled to be given at age 11 or 12 years also should receive vaccine. The ACIP encourages health care providers to administer a booster dose of to adolescents aged 11 to 18 years who have already received the recommended Td booster dose so they will be protected against pertussis as well as tetanus and diphtheria. Providers should not only educate adolescents and parents about the disease and the vaccines but also should participate in actively vaccinating this highly susceptible population with the newly available vaccine. As per ACIP recommendations, young adolescents, particularly those presenting for the 11- to 12-year-old well-examination, should have their immunization records reviewed and receive a booster vaccine if indicated. As noted earlier, most visits adolescents make to health care providers are for acute illnesses or injuries (Foundation for Accountability, 2001). Because the ACIP has determined that vaccination is not contraindicated during mild acute illness with or without a fever, such as diarrhea or mild upper respiratory tract infection, health care providers should not hesitate to assess adolescents vaccination status at each encounter to avoid missing opportunities to vaccinate (CDC, 2002a). CONCLUSIONS Adolescents face many health problems that require attention from health care providers. One of the ways health care providers can provide care for their adolescent patients is to ensure that they have received all of their recommended immunizations. A booster dose of pertussis vaccine is a new addition to the adolescent immunization schedule. Although diagnosis of pertussis often is overlooked in adolescents presenting with cough illnesses, adolescents can be the source of pertussis infection for infants, a population in which disease can be severe. Pertussis disease represents a significant economic burden because of direct medical costs and decreased productivity caused by missed school and work days. In the past 25 years, the overall incidence of pertussis has increased, especially in adolescents and adults. This increase is thought to be the result of waning immunity to pertussis following vaccination. DTap vaccine is part of the primary immunization series in infants, and vaccine recently was approved for use as a booster vaccine in adolescents and adults. The ACIP recommends replacing the current Td booster vaccine with vaccine in adolescents. is generally well tolerated and provides immunity to tetanus, diphtheria, and pertussis comparable to that produced by Td and DTaP vaccines. The shifting epidemiology of pertussis requires health care providers to become vigilant in guarding the immunization status of adolescents as well as they have been for children. REFERENCES ADACEL. (2005). Prescribing information. Aventis Pasteur Limited, Toronto, Ontario, Canada. Advisory Committee on Immunization Practices. (June 30, 2005). ACIP recommends adolescent vaccination for tetanus, diphtheria and pertussis vaccine [National Immunization Program press release]. Retrieved July 25, 2005 from jun2005.htm American Medical Association. (1997). 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