Differences in Reactogenicity and Antigenicity of Acellular and Standard Pertussis Vaccines Combined with Diphtheria and Tetanus in Infants
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1 THE JOURNAL OF INFECTIOUS DISEASES. VOL. 157, NO.4. APRIL by The University of Chicago. All rights reserved /88/574-13$1. Differences in Reactogenicity and Antigenicity of Acellular and Standard Pertussis Vaccines Combined with Diphtheria and Tetanus in Infants Edwin L. Anderson, Robert B. Belshe, and Julie Bartram From the Center for Vaccine Development, Departments of Medicine and Pediatrics, Marshall University School of Medicine, Huntington, West Virginia Clinical and serological responses of infants to primary immunization with diphtheriatetanus-pertussis (DIP) vaccine containing components of acellular pertussis vaccine(dip AC) were compared in a double-blind study with responses of infants receiving whole-cell DIP vaccine (DTP-WC). Three doses of either DIP-AC containing lymphocytosispromoting factor (LPF) and filamentous hemagglutinin (FHA) or DIP-WC vaccine were given to infants at two, four, and six months of age. Nineteen infants received DIP-AC vaccine, and 2 infants received DIP-WC vaccine. Significantly more infants who received DIP-WC vaccine manifested fever, swelling, and/or total reactions than did infants who received DTP-AC vaccine. Infants who received DIP-AC vaccine had comparable antibody titers to LPF and significantly higher titers to FHA after three immunizations, as compared with the infants who received DTP-WC vaccine (P ~.1). The DIP-WC vaccine stimulated higher pertussis agglutination titers (P =.4) than did DIP-AC. The DIP AC vaccine was immunogenic and significantly less reactogenic in infants than was the currently used DTP-WC vaccine. Pertussis continues to occurin the United States, although immunization against this disease has been standardpractice for rv4 y [1-6]. The currentlyused pertussis vaccine is effective [7, 8] but has been associated with adverse reactions, some of which are severe[9, 1].A direct relation between pertussis vaccination and rare, serious reactions has not been proved but has served to stimulate interest in the development of a less reactogenic vaccine. Japanese investigators have developed an acellular pertussis vaccine that contains lymphocytosis-promoting factor (LPF) and filamentous hemagglutinin (FHA); these Received for publication 11 June 1987 and in revised form 3 November The protocol for this study was approved by the Marshall University Institutional Review Board and the Clinical Research Committee of the National Institute of Allergy and Infectious Diseases. This work was supported by contract AI from the National Institute of Allergy and Infectious Diseases and by Wyeth Laboratories. We thank the infants' parents for their cooperation; Frances Crookshanks-Newman, Carol Berry, Sally Wells, Jill Taylor, and Arlene Napier for assistance and study coordination; and Drs. Marc Gurwith, John Gallo, Richard Hjorth, Mark Levner, and Steven Vernon (Wyeth Laboratories) for providing vaccine and laboratory support. Please address requests for reprints to Dr. Edwin L. Anderson, Department of Medicine, Marshall University School of Medicine, Huntington, West Virginia two antigens in combination induced protective antibody in animal studies [11]. The acellular vaccines have been reported to be safe and efficacious in Japanese children [11-13], and in studies in children from the United States, one of the acellular pertussis vaccines has been found to be safe and antigenic [14-16]. The first phase of pertussis infection is characterized by attachment of Bordetella pertussis to the ciliated epithelium of the respiratory tract, and the second phase of pertussis is thought to be a result of a toxin secreted by the organism [17, 18].The toxin has various names, including pertussis toxin, histamine-sensitizing factor, islet cell-activating protein, and LPF [19]. In addition to LPF, FHA is thought to have a role in the pathogenesis of pertussis through adherence, and antibody to FHA may have a role in immunity to pertussis. Both LPF and FHA proteins have been incorporated as components ofacellular pertussis vaccines in Japan and the United States [11-15]. LPFand FHAare protective against aerosol challenge with liveb.pertussis in animal models, but only LPF is protective against intracerebral challenge. Munoz et al. [2] found that vaccination with glutaraldehyde-detoxified LPF protected mice from death during intracerebral challenge with pertussis organisms. Odaet al. [21] demonstratedthat an acellular pertussis vaccine given to female mice resulted in protective activity that was transferred from Downloaded from at Penn State University (Paterno Lib) on March 6,
2 732 Anderson, Belshe. and Bartram mother mice to their offspring through milk and across placental membranes. In other studies [19], mice immunized intraperitoneally with FHA or detoxified LPFwereprotected afteraerosol challenge with live B. pertussis; intraperitoneal injection of LPF protected mice from intracerebral challenge, but FHA did not. Adherence of B. pertussis to ciliated epithelium appears to be a crucial step in the pathogenesis of respiratory disease [18, 22]. Tuomanen et al. [18] found that B. pertussis lost its ability to adhere to ciliated respiratory epithelium when either FHA or LPF was absent. Both LPF and FHA were bound to the surface of Bordetella strains and to respiratory cilia and appeared to act in concert as adhesins ofb. pertussis for human cilia. Stimulation of antibodies that block adherence of B. pertussis to respiratory epithelium may be an important attribute of candidate vaccines. We performed the present study to compare, in infants, the reactogenicity and antigenicity of the presently used whole-cell diphtheria-tetanus-pertussis (DTP) vaccine (DTP-WC) and an acellular pertussis-containing DTP vaccine (DTP-AC). In addition, this study was done to determine the response of infants to a primary immunization series with a DTP-AC vaccine manufactured by Wyeth Laboratories (Philadelphia) by using Takeda pertussis antigens. Subjects and Methods Volunteers and vaccine. Healthy two-month-old infants were recruited from participating private pediatric practices in the community of Huntington, West Virginia. A single lot of DTP-AC vaccine (control no ) provided by Wyeth Laboratories was used. The vaccinecontained 5.6 mouse-protective units/o.5-ml dose, 3 HA units ofpertussis component vaccine (Takeda vaccine [11]), 5. Lf (limit offlocculation units) of tetanus toxoid, and 7.5 Lf ofdiphtheria toxoid. Injections of.5 ml/dose were administered im into the anterior lateral thigh ofthe infants. Commercially available DTP-WC vaccine used in the study (Wyeth Laboratories) had a potency of at least 5.5 mouse-protective units/dose and had the same diphtheria and tetanus components as did the DTP-AC vaccine. Study design. Thirty-nine children were studied. Twenty of the children were given DTP-WC vaccine, and 19children received DTP-AC vaccine. The study was randomized and double-blinded, and coded vials of vaccine were provided by Wyeth Laboratories. Infants were vaccinated at two, four, and six months ofage. Infants experiencing reactions that contraindicated additional doses of DTP vaccine were subsequently given DT (diphtheria-tetanus) vaccine. Temperatures of children were taken at 3, 6, 24, 48, and 72 h after immunization. Visits were made daily for three days to the homes of vaccinees by vaccine center staff nurses to examine the vaccinees; visits were also made on days 7 and 14 after immunization. The nurses recorded temperature (rectal) and measured the amount of redness and swelling occurring at the injection site. Information on behavioral changes (fretfulness or unusual crying) and use ofantipyretic medication was also obtained. Respiratory secretions were obtained for culture of viruses and bacteria from children who manifested symptoms of respiratory illness. Laboratory studies. Serum was obtained by venipuncture before immunization and before each subsequent vaccination. Blood was also obtained one month after the third dose ofvaccine. Frozen specimens of cord blood were available for 19of the study infants. Serological studies were performed by Wyeth Laboratories. The serological response to tetanus immunization was determined by indirect HA [23]. Diphtheria antitoxin activity was determined by using a microtissue culture test with Vero cells [24]. Serological responses to tetanus and diphtheria toxoids wereconverted to internationalunits (IV). Antibody to pertussis was measured by agglutination of B. pertussis [25]. Antibodies to LPF and FHA were measured by ELISA using the method of Vernon et al. [26]. Statistics. y} Tests were performed to compare the occurrence of adverse reactions among the two groups of volunteers. Student's t test was used to compare antibody titers with antigens among the two age-groups of vaccinees. Results DTP-ACwas significantly less reactogenic than DTP WC (table 1). Temperatures >37.8 C, swelling >2 mm, and reactions that were other than mild occurred significantly more often after the first vaccination among infants who received DTP-WC vaccine than among those given DTP-AC vaccine. After the first immunization, four infants in the DTP-WCimmunization group had reactions that were consid- Downloaded from at Penn State University (Paterno Lib) on March 6, 216
3 Acellular Pertussis Vaccine in In/ants 733 Table 1. Occurrence of adverse reactions in the 48 h after vaccination with DTP-WC or DTP-AC at two, four, and six months of age. Immunization I Immunization 2 Immunization 3 All three immunizations DTP- DTP- DTP- DTP- DTP- DTP- DTP- DTP- Adverse WC AC WC AC DT WC AC DT WC AC DT reaction (n = 2) (n = 19) (n = 16) (n = 17)*(n = 5) (n = 14)t (n = 17) (n = 6)t (n = 5) (n = 53) (n = II) Rectal temp. >37.8 C Rectal temp. ~38.4 C 3 4 I 8 Any redness I Redness >2mm 3 I Any swelling Swelling >2 mm 6 I 3 9 I Pain 5 4 I I 1O Fretfulness I I 17# 7 Unusual crying** 3 5 Acetaminophen administered Moved to DT group 4 I I 5 I Any reaction Any reaction except mildtt 14 5 II # * One child was inadvertently given DTP-WC and was excluded from the study. t One child was moved to the DT group because he had Haemophilus injluenzae meningitis and seizures before immunization 3 was given. t One child in this group moved out of state before DT immunization 3 was given. For DTP-WC vs. DTP-AC, P <.1 by Fisher's exact test (immunizations 1,2,3) or by X' (all three immunizations). P for DT vs. DTP-AC was not significant. II One child was shedding parainfluenza virus type 3 and cytomegalovirus at the time of elevated rectal temp (temperature). # For DTP-WC vs. DTP-AC, P <.5, X' = 6.2. ** Unusual crying was defined as an infant whose crying or screaming lasted >1 h and who could not be consoled and would not nurse or feed from a bottle. tt Reactions that were not mild include temp ~38.4 C, redness or swelling>2 mm, pain at injection site, and fretfulness or crying. ered severe and subsequently received DT vaccine. Three of the infants manifested unusual crying, and one had severe local and systemic reactions. In contrast, only one DTP-AC vaccinee had a reaction severe enough to warrant subsequent vaccination with DT rather than DTP. After the second immunization, adverse reactions other than mild were significantly more common among the children receiving DTP-WC vaccine (P <.5). One additional child in the DTP-WCgroup manifested unusual crying; this infant subsequently was given DT vaccine. After the third immunization, there was no significant difference in adverse reactions between the two groupsof infants. Overall, significantly fewer infants given DTP-AC had adverse reactions after immunization than did infants given DTP-WC (36 of 53 vs, 45 of 5; X 2 = 7.46, P <.1). When mild adverse reactions were excluded, the difference in adverse reaction rates was even more pronounced (12 of 53 vs. 3 of 5; X 2 = 14.86, P <.1). Most infants were examined on days 7 and 14after vaccination for late onset of local reactions. Neither redness nor pain were noted in any vaccinee. Five of 18DTP-WCvaccinees and 1 of 19 DTP-AC vaccinees (P not significant) had palpable lumps >5 mm on day 7, and 3 of 17 DTP-WC vaccinees and none of the 12 DTP AC vaccinees had palpable lumps on day 14 after the third dose. There were significant differences in serological responses between the two groups of infants (figure Downloaded from at Penn State University (Paterno Lib) on March 6, 216
4 734 Anderson, Belshe, and Bartram <3 9 5.=goo ~. Z == 4. goo 88"...J -S88 «u '".. "' '" U l1OOO 2. '"888.~ 11 :J ~.goo Cord Blood Pre lmm. Post-lmm.. 1 Post lmm.. 2 Post lmm Months) 14 Months) 16 Months) )7 Months) Figure 1. Pertussis agglutination titers among infants who receivedeither standard DTP-WC vaccine(_) or DTP AC vaccine (). 1). Infants receiving DTP-WC vaccine had significantly higher pertussis agglutination titers after three injections than did infants given DTP-AC vaccine (P =.4). Furthermore, infants immunized with DTP-AC vaccine had pertussis agglutination titers significantly lower than their cord blood titers after three doses of vaccine (P =.1). Among the DTP- 1 5 E «1 8 "!9 '" II 8 I 5!l ~ 8 I 8 '8' I I 1 ITITERs s 11 (11 1 ) 16) IS) (11 11 IS) 1) ~ Cord Blood Pre-Imm. Post-Imm.vt Post-Imm. 2 Post-lmm Monthsl 14Months) 16Monthsl 17Monthsl Figure 2. Antibody titers to FHA among infants who werevaccinated with either standard DTP-WC (_) or DTP- AC vaccine (). 5!l E <, " 1 CXJ ::i 8 8 a 5 'f!l ~ I &, ITITERs s 1) (1) 13) 111 (11 14) 112) 1 ) (1) 1 ) 1 ) Cord Blood Pre-Imm. Post-Imm.. 1 Post-lmm. - 2 Post-Imm Monthsl 14Monthsl 16Months) 17Months) Figure 3. Antibody titers to LPF among infants vaccinated with either standard DTP-WCvaccine (_) or DTP AC vaccine (). WC vaccine recipients, there was no significant difference between cord blood agglutination titers and titers observed after completing primary DTP WC immunization. The DTP-AC vaccine stimulated equally high titers of antibody to LPF and significantly higher titers of antibody to FHA when compared with DTP-WC (figures 2 and 3). As with the other antigens in the vaccines, the nadir of antibody to LPF occurred at four months of age; by seven months of age, after vaccination with either DTP-AC or DTP-WC, antibody to LPF in the infants had been stimulated to levels found in cord blood. Antibody titers to FHA among DTP-ACvaccinees were significantly higher after the first vaccination (P =.2)than weretiters among DTP-WC recipients and remained higher throughout the immunization series (P <.1). Whole-cellpertussis antigen was not a requirement for the diphtheria and tetanus components to be antigenic (tables 2 and 3). After three immunizations, neither antibody titers to diphtheria toxoid (P =.7) nor antibody titers to tetanus (P =.26) were significantly different between the two groups of vaccinees, and all infants in both groups had >.1 IU of antitoxin/ml, the levelofantibody thought to be protective against tetanus and diphtheria [25, 26]. Discussion This is the first study in the United States in which infants were given a primary series of DTP vaccine 8 Downloaded from at Penn State University (Paterno Lib) on March 6, 216
5 Acellular Pertussis Vaccine in Infants 735 Table 2. Vaccine DTP-AC DTP-WC Serological response to diphtheria toxoid in infants vaccinated at two, four, and six months of age. Cord blood Preimmunization Postimmunization 1 Postimmunization 2 Postimmunization 3 (n = 11) (n = 18) (n = 18) (n = 15) (n = 16).25 (.7).4 (.1).2 (.4).7 (.1).2 (.4).23 (.9).5 (.1).1 (.2).8 (.4).52 (.2) NOTE. Data are expressed in IU/mL as the mean antibody titer ± SE. For DTP-AC vs. DTP-WC, antibody titers were not significantly different for each time that sera were obtained. containing FHA and LPF. In a preliminary study [16], we administered the Takeda DTP-AC vaccine to 6 infants and young children in an open trial, and the vaccine was significantly less reactogenic than reported for children in the United States who were receiving DTP-WC. In the present study, the DTP-AC vaccine was significantly less reactogenic than the DTP-WCvaccine in infants vaccinated at two, four, and six months of age. Excluding mild reactions (temperature <38.4 C and redness or swelling <2 mm), 67 of DTP-WCrecipients and 22.6% of DTP-ACvaccinees manifested adverse reactions. Ifall reactions are included, 9% and 67.9% of DTP-WC and DTP-AC vaccinees, respectively, had reactions. These reaction rates for DTP-WC vaccine were similar to rates reported, for infants, by other investigators [1, 29, 3]. Adverse reaction rates for the DTP-ACrecipients were similar to rates reported by Edwards et al. [14] and Lewiset al. [15] among older infants and young children but were higher than rates reported in Japan among children who are routinely vaccinated at two years of age [11, 32]. After the third dose, there was no difference in reaction rates between the two vaccine groups; this may have occurred because we removed five volunteers who manifested more-severe reactions to DTP-WC, and therefore, this group consisted only of children with little propensity to respond adversely to the vaccine. An unexpected proportionof infants in the DTP WC group had reactions that warranted vaccination with DT. Although the significance of unusual crying or screaming is unknown, the Committee on Infectious Diseases of the AmericanAcademy ofpediatrics considers persistent, unconsolable crying of ~3 h or unusual screaming a contraindicationto further pertussis immunizations. Although not all infants who were subsequently vaccinated with DT met this specific definition, we believed it was necessary to exercise caution. No infant had encephalopathy, convulsions, or shock/collapse, but our series was too small to expect the occurrence of one of these more serious adverse reactions. Differences in serological responses to the two vaccine groups occurredin our study. Pertussis agglutination titers among infants given DTP-AC in the present study were significantly lower than titers among infants receiving DTP-WC. This was in contrast to the higher titers among the six-month-old infants in our preliminary study who received DTP AC at six months of age but had received DTP-WC at two and four months of age (P <.5) [16]. This difference may be related to a smaller amount ofthe major agglutinogens in DTP-AC vaccine than are present in DTP-WC vaccine [13]. Whether lower agglutination levels will alter clinical efficacy is unknown. Japanese scientists [11-13] reported that the acellular vaccines were 78%-92% effective in preventing pertussis, an efficacy rate similar to the standard DTP-WC [1, 7, 8]. Antibody titers to LPF and FHA among DTP-AC vaccinees were greater than or equal to titers among DTP-WC recipients. The Downloaded from at Penn State University (Paterno Lib) on March 6, 216 Table 3. Vaccine DTP-AC DTP-WC Serological response to tetanus toxoid in infants vaccinated at two, four, and six months of age. Cord blood Preimmunization Postimmunization 1 Postimmunization 2 Postimmunization 3 (n = 11) (n = 17) (n = 18) (n = 15) (n = 16) 8.9 (2.44) 1.6 (.38).6 (.9) 2.1 (.41) 5.9 (1.17) 17.8 (9.14) 2.9 (.6) 1.1 (.35) 4.5 (3.26) 18.5 (7.77) NOTE. Data are expressed in IU/mL as the mean antibody titer ± SE. For DTP-AC vs. DTP-WC, antibody titers were not significantly different for each time sera were obtained.
6 736 Anderson, Belshe, and Bartram higher FHA titers among infants given DTP-ACwas not unexpected, because the Takeda acellular vaccine is an FHA-predominant preparation [13, 32], and the elevated FHAtiter may partiallyexplain the efficacy of the acellular vaccine reported by Japanese investigators [11-13]. In our preliminary trial [16], the postvaccination FHA titers among the sixmonth-old infants given a single dose of DTP-AC vaccine after receiving two previous doses of DTP WC were significantly lower than titers among infants given three doses of DTP-AC (P <.1). The presently used whole-cell pertussis vaccine has been extremely effective in reducing the incidence of pertussis. Serious reactions such as seizures, encephalitis, shock/collapse, permanent neurological sequelae, and death have been temporally associated with DTP vaccination, but a direct relation has not been established. These adverse reactions may be due to other causes. The DTP vaccine containing acellular pertussis components causes fewer reactions and gives a good antibody response to two potentially protective antigens. Further studies with the acellular pertussis vaccines in greater numbers of infants are needed. References 1. Broome CV, Fraser DW. Pertussis in the United States, 1979: a look at vaccine efficacy. 1 Infect Dis 1981;144: Pertussis-Maryland, MMWR 1983;32:297-3, Pertussis- Washington, MMWR 1975;34:39-4, Pertussis - United States, 1982 and MMWR 1984;33: Pertussis surveillance, MMWR 1982;31: Pertussis outbreak-oklahoma. MMWR 1984;33:2-4, Hinman AR, Koplan lp. Pertussis and pertussis vaccine. Reanalysis of benefits, risks, and costs. lama 1984;251: Koplan lp, Schoenbaum SC, Weinstein MC, Fraser DW.Pertussis vaccine - an analysis of benefits, risks and costs. N Engl 1 Med 1979;31: Miller DL, Alderslade R, Ross EM. Whooping cough and whooping cough vaccine: the risks and benefits debate. Epidemiol Rev 1982;4: Cody CL, Baraff LJ, Cherry ld, Marcy SM, Manclark CR. Nature and rates of adverse reactions associated with DIP and DI immunizations in infants and children. Pediatrics 1981;68: Sato Y, Kimura M, Fukumi H. Development of a pertussis component vaccine in lapan. Lancet 1984;1: Aoyama T, Murase Y,Kato T, Iwata T. Efficacy of an acellular pertussis vaccine in lapan. 1 Pediatr 1985;17: Noble GR, Bernier RH, Esber EC, Hardegree MC, Hinman AR, Klein D, Saah Al. Acellular and whole-cell pertussis vaccinesin lapan. Report of a visitby US scientists. lama 1987;257: Edwards KM, Lawrence E, Wright PF. Diphtheria, tetanus, and pertussis vaccine. A comparison of the immune response and adverse reactions to conventional and acellular pertussis components. Am 1 Dis Child 1986;14: Lewis K, Cherry ld, Holroyd Hl, Baker LR, Dudenhoeffer FE, Robinson RG. A double-blind study comparing an acellular pertussis-component DIP vaccine with a wholecell pertussis-component DIP vaccine in 18-month-old children. Am 1 Dis Child 1986;14: Anderson EL, Belshe RB, Bartram 1, Gurwith M, Hung P, Levner M, Vernon SK. Clinical and serologic responses to acellular pertussis vaccine in infants and young children. Am 1 Dis Child 1987;141: Pittman M. The concept of pertussis as a toxin-mediated disease. Pediatr Infect Dis 1984;3: Tuomanen E, Weiss A. Characterization of two adhesins of Bordetella pertussis for human ciliatedrespiratory-epithelial cells. 1 Infect Dis 1985;152: Oda M, Cowell ll, Burstyn DG, Manclark CR. Protective activities of the filamentous hemagglutinin and the lymphocytosis-promoting factor of Bordetellapertussis in mice. 1 Infect Dis 1984;15: Munoz 11, Arai H, Cole RL. Mouse-protecting and histaminesensitizing activities of pertussigen and fimbrial hemagglutinin from Bordetella pertussis. Infect Immun 1981; 32: Oda M, Izumiya K, Sato Y, Hirayama M. Transplacental and transcolostral immunity to pertussisin a mouse model using acellular pertussis vaccine. 1 Infect Dis 1983;148: Tuomanen EI, Hendley 1. Adherence of Bordetellapertussis to human respiratory epithelial cells. 1 Infect Dis 1983;148: Millian sr,cherubince, Sherwin R, Fuerst HT. A serologic survey of tetanus and diphtheria immunity in New York City. Arch Environ Health 1967;15: Miyamura K, Nishio S, Ito A, Murata R, Kono R. Micro cell culture method for determination of diphtheria toxin and antitoxin titres using VERO cells. 1. Studies on factors affecting the toxin and antitoxin titration. 1 Bioi Stand 1974;2: Manclark CR, Meade BD. Serological response to Bordetella pertussis. In: Rose NR, Friedman H, eds. Manual of clinical immunology. 2nd ed. Washington, DC: American Society for Microbiology, 198: Vernon SK, Wiener FP, Urbano C, Levner MH. An antigenconserving ELISA for detecting humanantibodiesto Bordetella pertussis filamentous hemagglutinin. 1 Bioi Stand 1986;14: McComb la, Dwyer RC. Passive-active immunization with tetanus immune globulin (human). N Engl 1 Med 1963; 268: Crossley K, Irvine P, Warren lb, Lee BK, Mead K. Tetanus and diphtheria immunity in urban Minnesota adults. lama 1979;242: Barkin RM, Samuelson ls, Gotlin LP. DIP reactions and serologic response with a reduced dose schedule. 1 Pediatr 1984;15: Barkin RM, Pichichero ME. Diphtheria-pertussis-tetanus vac- Downloaded from at Penn State University (Paterno Lib) on March 6, 216
7 Acellular Pertussis Vaccine in Infants 737 cine: reactogenicity of commercial products. Pediatrics 1979;63: Fredriksen JH, Freholm LO, Paulsen BS. Purification and preliminary characterization of agglutinogen 3 from Bordetellapertussis. In: Manclark CR, Hennessen W, eds. Developments in biological standardization. Vol 6. Proceed- ings of the Fourth International Symposium on Pertussis. Geneva: S. Karger, 1985: Aoyama T, Hagiwara S, Murase Y, Kato T, Iwata T. Adverse reactions and antibody responses to acellular pertussis vaccine. J Pediatr 1986;19:925-3 Downloaded from at Penn State University (Paterno Lib) on March 6, 216
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