The Spatial Dynamics of Poliomyelitis in the United States: From Epidemic Emergence to Vaccine-Induced Retreat, 1910–1971

Abstract

This article seeks to advance an understanding of the spatial dynamics of one of the great emergent viral diseases of the twentieth century—poliomyelitis. From an apparently rare clinical condition occurring only sporadically or in small outbreaks before the late nineteenth century, poliomyelitis had, by the early 1950s, developed into a globally distributed epidemic disease. But, from 1955, continued growth was suddenly and dramatically reversed by the mass administration of inactivated (killed) and live (attenuated) poliovirus vaccines. After almost half a century of vaccine control, the world now stands on the brink of the global eradication of the disease. Against this background, the article draws upon information included in the U.S. Public Health Service's Public Health Reports and the U.S. Centers for Disease Control and Prevention's Morbidity and Mortality Weekly Report to examine the spatial dynamics of poliomyelitis during the phases of epidemic emergence (1910–1955) and vaccine-induced retreat (1955–1971) in the United States. It is shown that epidemic emergence was accompanied by shifts in the spatial center of activity from early diffusion poles in the northeastern states, to the western seaboard, and then finally to cover all the states of the Union. This was accompanied by accelerating epidemic propagation. The introduction of mass vaccination from the mid-1950s realigned spatial transmission of the disease, producing increased spatial volatility in the geographical center of activity and heightened dependence of epidemic outbreaks upon endemic reservoirs in the most populous states. Finally, the empirical results are generalized to suggest that the emergence and reemergence of many infectious diseases is a distinctively geographical process.

Key Words:

• emerging diseases
• epidemics
• poliomyelitis
• spatial diffusion
• United States of America

Acknowledgements

The work described has been undertaken as part of a five-year program of research entitled Historical Geography of Emerging and Re-Emerging Epidemics, 1850–2000, funded by the Wellcome Trust. The additional support of the Economic and Social Research Council (BT) and the Leverhulme Trust (MS-R) is gratefully acknowledged. The authors also wish to express their thanks to Cathryn Nettleton, who encoded some of the data examined in the present work, and to the referees for their helpful comments on an earlier draft of the article.

Notes

Source: Based on information in Holt and Bartlett (1908, 656–61), Batten (1911, 220–1), and Lavinder, Freeman, and Frost (1918, Table 1, 27–9).

¹July 1910–May 1955.

²June 1955–December 1971.

³July 1910–December 1971.

Source: State-level notifications included in the Public Health Reports (Washington, DC: Government Printing Office, 1910–1951) and Morbidity and Mortality Weekly Report (Atlanta, GA: Centers for Disease Control, 1952–1972).

Source: after Cliff, Haggett, and Ord (1986, 199–201).

1. John R. Paul, address to the Second International Conference on Poliomyelitis, Rome, 1952, cited by Dave (1960, 338).

2. For a useful overview of progress toward the global eradication of poliomyelitis, including a consideration of the major obstacles to the interruption of wild poliovirus transmission in the persistent reservoirs of Nigeria, India and Pakistan, see World Health Organization (2003).

3. Beginning with the years 1933–1937, C. C. Dauer—sometime medical advisor of the National Office of Vital Statistics, U.S. Public Health Service—produced a long-running series of maps of annual poliomyelitis incidence in the counties of the U.S. The maps appeared in successive volumes of the U.S. Public Health Reports (1938–1955), eventually terminating with the national map for 1954. In a generous acknowledgement of his deceased colleague, Dauer (1953, 1034) credited the late L. L. Lumsden as the original inspiration behind the map series. See, also, Lumsden (1938).

4. In the present article, the term endemic is used to refer to an infectious agent that is constantly circulating, to a greater or lesser degree, among persons of a certain class or among persons resident in a particular locality. The term epidemic is used to refer to a widespread outbreak of an infectious agent that, in the instance of poliovirus, is usually associated with the occurrence of multiple cases of clinical disease.

5. Bell (1844) did not record the exact date of the epidemic on St. Helena, although it is likely to have occurred within the period 1831–1835; see Paul (1971, 43).

6. According to Schonberger et al. (1984, S424), the successful control of paralytic poliomyelitis through the U.S. mass vaccination program, 1955–1981, involved the net distribution of ∼483 million doses of inactivated poliovirus vaccine (IPV), ∼114 million doses of each of three types of monovalent oral poliovirus vaccine (MOPV), and ∼423 million doses of trivalent oral poliovirus vaccine (TOPV). The majority of doses of IPV were distributed between 1955 and 1962, with a subsequent switch to MOPV (1962–1964) and TOPV (1965 ff.) as the vaccine of choice. More recently, because of the risk of reversion of attenuated virus to neurovirulence, coupled with a desire to remove all poliovirus from circulation, the U.S. reintroduced IPV (in enhanced potency form) as part of a mixed IPV–OPV routine schedule in 1995. From January 2000, an all-IPV schedule was implemented as the strategy of choice for routine childhood vaccination in the U.S. (see Anonymous 1999; Sutter, Prevots, and Cochi 2000; Swennen and Levy 2001).

7. Between 1980 and the certification of eradication of poliomyelitis in the Americas (1994), a total of 133 confirmed cases of paralytic poliomyelitis were recorded in the U.S. Of these, 125 were associated with the administration of oral poliovirus vaccine, six were classified as imported, and two were of indeterminate origin (CDC 1997b).

8. Our decision to limit the present analysis to the level of state was conditioned by the availability of a near-complete and unbroken series of poliomyelitis counts for the entire period of systematic reporting in the Public Health Reports and Morbidity and Mortality Weekly Report. Although both publications do include data on finer spatial scales (large cities/metropolitan areas), analysis of the latter data was precluded by both (i) the fragmentary nature of the available disease record and (ii) statistical instabilities associated with small disease counts in many areas. Finally, although poliomyelitis counts for the nearly 3,100 counties of the U.S. formed the basis of a series of annual maps by Dauer in the 1930s–1950s (see Note 3), a systematic examination of the library and archives of Centers for Disease Control and Prevention (CDC) has failed to yield any evidence of the routine and centralized publication of poliomyelitis data at this spatial scale.

9. On 9 August 1910, the U.S. Surgeon-General, Walter Wyman, forwarded a missive to the secretaries of the state and territorial boards of health in order to ascertain “as accurately as possible the general prevalence and geographic distribution of anterior poliomyelitis (infantile paralysis) in the United States” (U.S. Public Health and Marine Hospital Service 1911, 1347). The following month, with state-level counts of poliomyelitis morbidity and mortality for July 1910 now secured, a second communication (dated 20 September 1910) requested the executive officers of the state and territorial boards of health and health departments to forward to the Surgeon-General's Office “a monthly memorandum of the course of the disease … beginning with the month of August [1910] … This will be supplemental to and a continuation of the information requested in bureau letter of August 9” (U.S. Public Health and Marine Hospital Service 1911, 1350).

10. U.S. Public Health and Marine Hospital Service (1911, 1347–50).

11. The nonconterminous states of Alaska and Hawaii were excluded from the present analysis on account of the fractured nature of the early records of poliomyelitis notifications.

12. In order to reconcile the monthly (1910–1926) and weekly (1927–1971) reporting intervals, cases reported on a weekly basis were assigned to the month in which the last day of the reporting week fell. This technique has been used before in historical studies of infectious diseases (Cliff, Haggett, and Smallman-Raynor 1998a, 117) and has the advantage of providing a simple and unambiguous method for assigning data to a coarser temporal scale.

13. The manifest difficulties of the variable inclusion of nonparalytic cases in official poliomyelitis totals were highlighted by Albert B. Sabin in his contribution to the First International Poliomyelitis Conference (New York, 1948). As Sabin (1949, 3) explained: Since there are as yet no simple, readily applicable tests for poliomyelitis infection, the recognition of the nonparalytic forms is fraught with great uncertainty and is continuing to be an uncontrollable and confusing variable in all statistical analyses of the disease. There are good reasons for believing that the nonparalytic cases which are reported, represent only a small fraction of the total number of minor illnesses caused by poliomyelitis virus, and it seems to me more harmful than useful to have them included without qualification in statistical reports of the disease.

14. Although caution must be exercised in the use of above-average incidence as a criterion for the identification of epidemic intervals (Gilliam, Hemphill, and Gerende 1949b), preliminary analysis indicated that the principal effect of a systematic increase in the epidemic threshold from z=0 (39 epidemics) to 0.5 (30 epidemics), 1.0 (21 epidemics), and 1.65 (15 epidemics) was to screen out the lower-magnitude events in the pre-1930 and post-1955 periods (Table 3). Given the apparent temporal nonstationarities associated with the epidemic generating mechanism in Figure 1, the lower epidemic threshold (z=0) was applied to avoid omission of events of marked contemporary significance in the tails of the disease curve in Figure 1.

15. According to the U.S. Bureau of the Census (1971, 7), the period 1910–1971 was associated with a modest westwards shift in the center of the U.S. population, from southern Indiana to southwestern Illinois.

16. Trevelyan, B., M. Smallman-Raynor, and A. D. Cliff. The spatial structure of epidemic emergence: The 1916 poliomyelitis epidemic in the United States. Journal of the Royal Statistical Society (in review).

17. Smallman-Raynor, M., A. D. Cliff, R. P. Haining, and B. Trevelyan. Detecting space-time clusters of infectious diseases: Using a scan statistic to map the incidence of the 1916 poliomyelitis epidemic in the northeastern United States. American Journal of Epidemiology (in review).

18. We note that the first-order nearest neighbor graph, which yields a relatively sparse network, is just one of several graphs that could be specified for the assessment of spatial contagion (Cliff et al. 1975; Haggett 1976). As described by Haggett (1976), for example, a simple adjacency graph (formed on the basis of the contiguity of state boundaries), suitably weighted according to geographical separation, length of shared boundary, or some measure of population interaction, would provide an alternative test bed for the operation of contagious diffusion.

19. In fact, available evidence indicates that the state population hierarchy displayed a remarkable degree of stability over the 738-month observation period, 1910–1971. To illustrate this, state population estimates for seven sample years [1910 (10) 1970] were ranked from largest (rank 1) to smallest (rank 49) and systematically compared using Spearman's rank correlation coefficient, r_s . The resulting 7 × 7 correlation matrix yielded a mean association () of 0.96, with the extreme points of the sample (1910 and 1970) marked by a highly significant and positive correlation (r_s =0.90; p<0.001 in a one-tailed test).

20. For the seven sample years, the correlation analysis yielded the following values of r: 0.93 (1910); 0.94 (1920); 0.95 (1930); 0.96 (1940); 0.98 (1950); 0.99 (1960); 0.99 (1970).

21. Not least, the spatial transmission of poliomyelitis did not appear to follow the patterns of human communication ordinarily observed for infectious diseases of childhood. As Dauer (1938) observed, There have been a number of statements in the literature regarding the tendency of poliomyelitis to spread along lines of human traffic. However, there is no evidence of such manner of spread to be found in the data used here. Geographical barriers such as mountains, valleys, and large rivers, do not seem to have influenced the direction in which the disease spreads (1019).

22. To meet the assumption of temporal stationarity in the time series under analysis (Chatfield 1989), regression techniques were used to detrend all series prior to the computation of the cross-correlation functions.

23. One complication of the present analysis is that, unlike the parameters b ₁ and b ₂, the quantities and s are not dimensionless and reflect the length of the particular epidemic under analysis. Consequently, to allow comparison between epidemic events, the values of and s in Figure 8 have been scaled by the duration (in months) of the corresponding epidemics.

24. See Note 3.

25. See Notes 16 and 17.