Background and History

Poliomyelitis is an acute infectious disease caused by an enterovirus. There are three types of this virus: types 1, 2, and 3. Each type is capable of infecting humans; there is no cross-immunity and only those individuals immune to each of the three types are protected against all three types. The virus enters the body by the oral or respiratory route and multiplies in the pharynx and small intestine. Within 24 hours it invades the regional lymph nodes, and after an additional 24 to 48 hours it enters the bloodstream, which carries it to the secondary sites of replication in many organs, and thus, viremia develops and is maintained and enhanced. During the period of viremia, the virus can reach the central nervous system and initiate infection there. Antibodies appear within 1 week to 10 days after the initial infection, and viremia then ceases, probably as a consequence of neutralization by the antibodies. Only 1 to 2 percent of infected individuals develop disease in the central nervous system, and fewer still have residual paralysis. Nevertheless, the portent of these rare consequences is great, because they result in death or lifelong disability.

Although there are currently effective vaccines against poliovirus, even before they became available, Hammon et al. (1953) demonstrated the effectiveness of passive immunization by injections of pooled gamma globulin. Various attempts at developing a vaccine had been thwarted by the absence of an effective in vitro system of virus replication. The establishment in 1949 of the tissue culture technique for supporting virus growth made development of a vaccine possible (Enders et al., 1949). It was for these findings that J.F. Enders, F.C. Robbins, and T.H. Weller received the Nobel Prize in 1954. This development was followed by efforts to generate sufficient quantities of the virus to inactivate it and use it as an inert antigen. An alternative approach was to attenuate the wild-type virus and render it safe as a replicating antigen. Both were successful and today there are two forms of the vaccine: the inactivated polio vaccine (IPV), which is administered by the parenteral route, and the live attenuated vaccine, which is administered orally and hence is known as the oral polio vaccine (OPV).

IPV was developed in 1953 by Jonas Salk (Salk, 1953; Salk et al., 1953); OPV was developed by Koprowski and colleagues (1952), who were the first to use it, and Albert Sabin (1956). An enhanced-potency IPV was developed in the late 1970s and is used today. Currently, IPV and the Sabin strains of OPV are available for use in the United States; however, OPV is the vaccine recommended for general use and is the most prevalent (American Academy of Pediatrics, Committee on Infectious Diseases, 1991).

Shortly after the licensure of IPV in 1955, the vaccine manufactured by Cutter was found to cause paralytic disease. It contained residual infectious virus. The reason was traced to the method of inactivation. At that time the dynamics of the inactivation process were not fully understood, and the U.S. government's requirements for vaccine production were ambiguous. All of these problems have since been corrected.

The first OPV was licensed in 1960 after an extensive trial in the former Soviet Union (Benison, 1982). By then, over 100 million people in the former Soviet Union and Eastern Bloc countries—except Poland—had received the Sabin vaccine (LaForce, 1990). Trials of OPV in the United States followed, and monovalent OPVs were quickly licensed. The trivalent OPV used today was licensed in 1963. In the 1962 recommendations of the U.S. Public Health Service, no preference for one or the other form of the vaccine was expressed (U.S. Public Health Service, 1962), but in 1964 the Committee on Infectious Diseases of the American Academy of Pediatrics recommended the use of OPV.

Polio has been eliminated as an endemic disease in the United States and many developing countries. Outbreaks have occasionally occurred in subsets of unvaccinated susceptible individuals. A persistent concern has been the possibility of the rare complication of paralytic poliomyelitis in vaccinees and their contacts, particularly those with impaired immunity. This is discussed in detail later in this chapter. Some countries, for example, Denmark, use a mixed schedule of IPV followed by OPV. Other nations, such as Finland and Holland, continue to rely on IPV. The debate over the relative efficacy of OPV versus that of IPV continues in the literature, as does debate regarding the use of combined schedules of IPV and OPV (Institute of Medicine, 1977, 1988).

The American Academy of Pediatrics and the Advisory Committee on Immunization Practices recommend that OPV be administered at ages 2, 4, and 15 months and again at ages 4 to 6 years. If IPV is used, it should be given according to the same schedule as OPV.

Biologic Events Following Immunization

Each of the three immunologically distinct types of poliovirus—types 1, 2, and 3—can cause paralytic disease. Both IPV and OPV stimulate immune responses against all three types of virus. OPV induces gastrointestinal mucosal immunity to a greater degree than IPV. The enhanced-potency IPV used today in the United States produces a humoral antibody response superior to that of OPV (Onorato et al., 1991). It is not clear whether either OPV or IPV confers lifelong immunity (Nishio et al., 1984). The mechanism of attenuation of the neurovirulence and that of occasional reversion to neurovirulence have been described in detail in a recent review (Racaniello, 1992). Recipients of OPV shed the virus in their feces, and contacts exposed to the virus can become infected.

Poliomyelitis

History of Suspected Association

The association between live attenuated polio vaccine and cases of paralytic poliomyelitis dates back to the time of administration of the first live attenuated polio vaccine tried by Kolmer in the 1930s (Kolmer, 1936). Leake (1935) described nine cases of poliomyelitis that occurred following vaccination with the Kolmer vaccine and that seemed to be caused by the vaccine. The concept that live attenuated polio vaccine causes a small number of poliomyelitis cases thus has a history of at least six decades.

Shortly after licensing of Sabin's OPV, the United States Communicable Diseases Center (CDC; later named the Center for Disease Control, the Centers for Disease Control, and, more recently, the Centers for Disease Control and Prevention) reported its monitoring of vaccine-associated cases of paralytic polio. Henderson et al. (1964) summarized data for the United States collected by the CDC in 1962, 1963, and 1964. They evaluated 123 cases of paralytic polio that had occurred within 30 days of OPV administration and decided that 57 cases were compatible with vaccine-induced disease. Fifteen of the cases occurred after receiving the type 1 vaccine, with an estimated incidence of 0.17 case per 1 million doses. Thirty-six cases occurred following vaccination with the type 3 vaccine, with an incidence of 0.40 case per 1 million doses. Two cases occurred following vaccination with the type 2 vaccine, and four cases occurred following vaccination with the trivalent vaccine. The authors also described three cases of poliomyelitis that occurred in contacts of a recipient of the type 3 vaccine, but it is not clear whether the contact cases were included in the overall counts of vaccine-associated cases. Following publication of the paper by Henderson et al. (1964), case reports documenting vaccine-associated paralytic polio in recipients and contacts of recipients continued to appear. Table 7-1 summarizes the early case reports that described vaccine-associated poliomyelitis. By 1966, Chang et al. described a case of poliomyelitis in a 7-year-old recipient who was then found to have hypogammaglobulinemia. In 1966, Morse et al. documented a case of poliomyelitis in an unimmunized mother of a vaccinated infant. This was similar to the case of polio in an unimmunized father of a recently vaccinated infant reported by Swanson et al. (1967). Two reports provided evidence that contacts other than the parents or household members were also at risk of contracting polio. Balduzzi and Glasgow (1967) and Stolley et al. (1968) described unimmunized children who developed poliomyelitis after contact with recently vaccinated playmates or classmates.

TABLE 7-1

Early Reports of Vaccine-Associated Poliomyelitis, Published Before 1970.

Evidence for Association

Biologic Plausibility

OPV consists of live attenuated viruses that multiply in the intestinal tract and that can revert to a more virulent form, causing disease. A vaccine recipient excretes live virus for several weeks, and recipients or contacts may become infected with the virus.

Case Reports, Case Series, and Uncontrolled Observational Studies

Since the 1960s there have been about 100 studies reporting individual cases, case series, and national surveillances of vaccine-associated cases of paralytic poliomyelitis. Case definitions have been well developed by the CDC and the World Health Organization (WHO); a case of vaccine-associated paralytic poliomyelitis is said to occur in recipients if the onset of the disease begins 7-30 days postvaccination and is said to occur in contacts of vaccine recipients if the onset of the disease begins 7-60 days after a recipient's vaccination. Laboratory tests can identify the strain of the infecting virus as a wild-type or vaccine strain of poliovirus. The cases described above in the section History of Suspected Association are typical of those that followed in the 1970s and 1980s.

WHO and CDC have used standard definitions of cases of paralytic poliomyelitis for almost 30 years, and many nations have implemented polio surveillance systems to monitor their polio immunization programs. Table 7-2 summarizes national data from the United States, England and Wales, Belgium, Spain, Romania, Hungary, Italy, and northern Greece. Despite differences in the ways that data are categorized and reported and the changes in the incidence of polio from 1959 to the present, all the national data show a low incidence of vaccine-associated paralytic polio, on the order of a few cases per 1 million doses given or a few cases per 1 million vaccine recipients. The CDC data for the years 1975 to 1984 show an incidence of 1 case of vaccine-associated paralytic polio per 3.22 million doses of OPV distributed (Centers for Disease Control, 1986; Nkowane et al., 1987). When cases among immunodeficient recipients and contacts and patients with vaccine-like virus are included, the incidence is 1 case per 2.64 million doses of OPV distributed (Centers for Disease Control, 1986; Nkowane et al., 1987). The incidence is greater with the first dose of vaccine. The CDC has estimated that the overall dose-related incidence is 1 case per 520,000 first doses distributed versus 1 case per 12.3 million subsequent doses distributed (Nkowane et al., 1987).

TABLE 7-2

National Surveillance Studies of Polio.

The Monitoring System for Adverse Effects Following Immunization (MSAEFI) does not list poliomyelitis as a separate adverse event, although it may be included under categories such as "other neurologic symptoms," "other reactions," and "serious events.'' The Vaccine Adverse Event Reporting System (VAERS) contains several reports (submitted between November 1990 and July 1992) that may be cases of poliomyelitis, but the data are generally insufficient to state whether a case of vaccine-associated polio has occurred. Of the eight VAERS reports suggestive of vaccine-associated poliomyelitis, six provided insufficient information, one provided enough information to rule out vaccine-associated poliomyelitis (the time interval exceeded WHO guidelines), and one report provided information sufficient to be a well-documented case of vaccine-associated poliomyelitis. The report, which was filled out by a physician, stated, "Vaccine associated paralytic poliomyelitis confirmed by box 12 oligonucleotide sequencing of type III viral isolate. Occurred in an unvaccinated contact of a recently vaccinated eight-month old."

The data regarding OPV-related nonparalytic polio are more scarce than those for paralytic disease. A report of poliomyelitis surveillance in England and Wales from 1969 to 1975 documented 44 cases of nonparalytic poliomyelitis (Smith and Wherry, 1978). (Included in this definition were patients with a clinical diagnosis of nonparalytic poliomyelitis, as well as those with encephalitis or aseptic meningitis who also had cultural or serologic evidence of poliovirus infection.) Twelve of those cases were believed to have been associated with administration of OPV (11 in recipients, 1 in a contact). Poliovirus was isolated from 8 of the 11 recipient cases. All of the viruses were typed as the vaccine strain on the basis of reproductive capacity temperature (RCT) tests. Virus isolated from the one contact case was also typed as the vaccine strain. The authors calculated incidence rates of 0.1 per 1 million population at risk per year for both the paralytic and nonparalytic forms of disease. The authors noted that the definition of nonparalytic disease was, perhaps, broad, and thus, this represents an estimate of the highest possible number of nonparalytic cases. Poliovirus was isolated from recently vaccinated patients in the former West Germany between 1965 and 1970 (Thraenhart and Kuwert, 1972). Of the 34 patients with aseptic meningitis, virus isolated from 17 patients was typed by the RCT test as vaccine strain, from 13 patients as wild-type, and from 4 patients as intermediate. A study of the incidence of aseptic meningitis in Olmsted County, Minnesota, from 1950 to 1981 reported that 2 of the 283 patients with aseptic meningitis had received polio vaccine within 4 weeks prior to the onset of symptoms (Beghi et al., 1984). However, no mention of virus isolation was made, and the disease cannot be ascribed to the vaccine.

Controlled Observational Studies

None.

Controlled Clinical Trials

None.

Risk-Modifying Factors

The immune status of a vaccine recipient or a contact of a vaccine recipient modifies the risk of polio as an adverse event associated with OPV vaccination. Among OPV recipients, various types of immunodeficiency are often diagnosed after a patient develops polio after immunization with OPV. These cases are described in Table 7-3. Nonimmune contacts are at increased risk of developing polio after exposure to a person immunized with OPV. These cases are described in Table 7-4. Most of the case reports describe unimmunized contacts who contracted polio, but two case reports describe immunodeficient contacts who contracted polio. For both vaccine recipients and their contacts, case reports may or may not be representative of the vaccine-associated cases of polio that occur in immunodeficient people. The CDC reports its cases of polio among immunodeficient people without categorizing the case as contacts or recipients (Centers for Disease Control, 1984, 1986). Unimmunized siblings and playmates of recipients continue to be at risk of contracting polio and may constitute a special risk group. With the increasingly younger age of entry into day care, there is a growing group of nonimmunized infants who may be exposed to infants recently immunized with OPV. The committee's review uncovered case reports of two infants, ages 20 days and 4 months (Bergeisen et al., 1986; Wilson and Robinson, 1974), who were unimmunized and who contracted polio from contact with a care giver and other infants.

TABLE 7-3

Cases of Polio Among Immune-Deficient Recipients.

TABLE 7-4

Cases of Polio Among Nonimmune Contacts of Polio Recipients.

Transverse Myelitis

Evidence for Association

Biologic Plausibility

Chapter 3 contains a discussion of the biologic plausibility for a causal relation between demyelinating disorders and vaccines in general.

Case Reports, Case Series, and Uncontrolled Observational Studies

Table 7-5 summarizes the three cases of transverse myelitis that have been reported in the literature to occur following vaccination with OPV. Two cases occurred in infants. A seven-month old girl developed symptoms 6 days after receiving OPV and diphtheria and tetanus toxoids (DT) (Whittle and Roberton, 1977). A 20-month girl developed symptoms 1 month after receiving OPV and diphtheria and tetanus toxoids and pertussis vaccine (DPT). She was found to be hypogammaglobulinemic (Douglas and Anolik, 1981). The third case occurred in a 24-year-old woman who was simultaneously vaccinated with OPV and typhoid and cholera vaccines (D'Costa et al., 1990). The woman had a fever at the time of vaccination and had an upper respiratory tract infection and pharyngitis for the 5 weeks preceding vaccination. The committee is aware of a case of transverse myelitis in a child with severe combined immunodeficiency syndrome (Richard B. Johnston, Yale University, New Haven, personal communication, 1993). Vaccine-strain poliovirus was isolated from the myocardium. VAERS listed two cases (submitted between November 1990 and July 1992) of transverse myelitis that occurred in patients after receiving a combination of DPT, OPV, and Haemophilus influenzae type b (Hib) vaccine and a combination of DPT, OPV, measles-mumps-rubella vaccine (MMR), and Hib vaccine, but the temporal and clinical details are insufficient for proper evaluation. Another VAERS report of transverse myelitis was a duplicate of the case report published in 1990 and discussed above (the 24-year-old woman). In addition, at a public meeting held in January 1993, the committee heard about a 4-month-old girl who developed transverse myelitis, diagnosed by neurologists, a few days after her second DPT and OPV immunizations. This was thought by the physicians treating the girl to be related to her immunizations (see Appendix B).

TABLE 7-5

Reports Associating Transverse Myelitis with Polio Vaccine.

Controlled Observational Studies

None.

Controlled Clinical Trials

None.

Guillain-Barré Syndrome

Evidence for Association

Biologic Plausibility

Chapter 3 contains a detailed discussion of the arguments that vaccines can cause demyelination, including GBS. There are no additional data demonstrating the biologic plausibility of a specific relation between polio vaccines and GBS.

Case Reports, Case Series, and Uncontrolled Observational Studies

Grose and Spigland (1976) describe a 10-month-old girl who developed GBS 4 to 7 days after receiving measles vaccine, DPT, and OPV. Poliovirus type 1 was isolated from a throat swab. The authors attributed the disease to the measles vaccine.

Leneman (1966) reviewed the literature prior to 1966 and described 1,100 case reports of GBS published between 1949 and 1966. In five cases, vaccination with IPV was mentioned, although the time interval between vaccination and the onset of GBS was not described. Changes in diagnostic procedures since 1949 might also disqualify some of the cases included in that summary. This secondhand summary of case reports does not supply sufficient information to determine whether IPV is associated with GBS.

In a study in Sweden, which utilized IPV exclusively, Andersen and Eeg-Olofsson (1976) discussed 10 cases of GBS that occurred in 1971 in individuals less than 60 years of age. In nine of the individuals, the onset of GBS occurred more than 1 year after a vaccination with IPV. The authors concluded that there was no association between IPV and GBS.

Data from the MSAEFI noted 14 cases of GBS following OPV administration from 1979 to 1990. In most cases OPV was given in combination with DPT, or MMR, or both. VAERS listed two cases of GBS (submitted between November 1990 and July 1992) following administration of OPV in combination with DPT and either MMR or Hib vaccine.

Controlled Observational Studies

Two controlled studies examined the association between GBS and polio vaccine (Table 7-6).

TABLE 7-6

Reports Associating Guillain-Barré Syndrome with Polio Vaccines.

The first study took place in a southern province of Finland (Uusimaa), where continuing surveillance of GBS from 1981 to 1986 uncovered an increase in the incidence of GBS following a nationwide program of immunizing children and adults against polio (Kinnunen et al., 1989). At that time, Finland generally used IPV, but an outbreak of 10 cases of poliomyelitis between August 1984 and January 1985 led to the decision to carry out a mass immunization with OPV. Ninety-four percent of the Finnish population was vaccinated with OPV during a 5-week period between February 10 and March 15, 1985. During and shortly after the immunization campaign, hospitals in the southern province, Uusimaa (population, approximately 1.17 million), received an unexpectedly high number of patients with GBS. The first and second quarters of 1985 showed a statistically significant higher number of cases of GBS than were found in the other quarters of the observational period. Over the 6-year period from 1981 to 1986 (including the period of OPV immunization), the mean number of cases of GBS per quarter was 3, and Kinnunen estimated a crude annual incidence of 1 case per 100,000 population. This is significantly higher than the mean for the 6-year period. Ten cases occurred in the first quarter and 6 cases occurred in the second quarter of 1985, the times corresponding to the immunization campaign. Ten patients were diagnosed with GBS within 10 weeks after vaccination with OPV, with the mean time of onset occurring at 31 days postvaccination. Six of the cases occurred within 6 weeks of vaccination. All patients with suspected GBS were evaluated separately by two neurologists, and consensus on the diagnosis was reached in every case. The patients' ages ranged from 15 to 73 years.

The study in Finland took advantage of two unique phenomena: a continuing surveillance of GBS that identified cases in the population over a 6-year period and a national program of immunizing adults in a 5-week period. The data showed an increase in the number of cases of GBS temporally associated with the immunization program, and the increase was statistically significant. The diagnosis of GBS was made by using consistent criteria throughout the observation period because of the prospective study on GBS that was in place well before the polio epidemic and immunization against polio occurred.

The study in Finland presents evidence that OPV may be associated with GBS and raises the question of why there have not been other reports of GBS associated with OPV. One explanation may be that the rarity of GBS, the usual predominance of GBS in adults, and the rarity of administration of OPV to adults have not produced any recognized cases of OPV-associated GBS. Kinnunen et al. (1989) estimated a crude annual incidence of 1 case of GBS per 100,000 population. The 10 cases that were considered vaccine associated occurred in patients ages 15 to 73 years. Six of the patients were in their 50s and two were in their 30s. If GBS mainly occurs in adults and relatively few adults receive OPV, the probability of uncovering a case of OPV-associated GBS without a surveillance system is low.

At the same time that Kinnunen et al. (1989) published the results of their study, Uhari et al. (1989) published a letter describing a cluster of GBS cases in children in Finland. They identified 27 cases of GBS in children ages 0.4 to 14.3 years over the 7-year period from 1980 to 1986, with an average incidence of 3.9 cases per year. They also noted a peak of 10 cases in 1985, which was different from the number of cases noted in other years, and the difference was statistically significant (P = 0.0042). Unlike Kinnunen et al. (1989), Uhari and colleagues did not confirm that the children with GBS had actually received OPV within the 6 weeks prior to the onset of GBS. They demonstrated an ecologic and temporal association between the OPV campaign and the cluster of GBS cases.

Controlled Clinical Trials

None.

Anaphylaxis and Thrombocytopenia

Death

A detailed discussion of the evidence regarding death following immunization can be found in Chapter 10. Only the causality argument and conclusion follow. See Chapter 10 for details.

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