See discussions, stats, and author profiles for this publication at: https://www.researchgate.

net/publication/14015059

Unimmunized Gypsy Populations and Implications for the Eradication of

Poliomyelitis in Europe

Article  in  The Journal of Infectious Diseases · March 1997

DOI: 10.1093/infdis/175.Supplement_1.S86 · Source: PubMed

CITATIONS READS

25 38

6 authors, including:

Barbara Ridolfi Francesco Forastiere

Istituto Superiore di Sanità Regional Health Service, Lazio
47 PUBLICATIONS   707 CITATIONS    865 PUBLICATIONS   25,939 CITATIONS   

SEE PROFILE SEE PROFILE

Some of the authors of this publication are also working on these related projects:

Radon exposure: epidemiology and risk evaluations View project

Health assessment in contaminated sites View project

All content following this page was uploaded by Barbara Ridolfi on 31 May 2014.

The user has requested enhancement of the downloaded file.

 S86

Unimmunized Gypsy Populations and Implications for the Eradication

of Poliomyelitis in Europe
R. Bruce Aylward, Daniela Porta, Lucia Fiore, Global Programme for Vaccines and Immunization, World Health
Barbara Ridolfi, Patrizia Chierchini, Organization, Geneva, Switzerland; Osservatorio Epidemiologico,
Regione Lazio, and Department of Virology, Istituto Superiore di San ita,
and Francesco Forastiere
Rome, Italy

The certification of poliomyelitis eradication in Europe will eventually require that countries
demonstrate there is a minimal risk of wild poliovirus reintroduction and sustained transmission
through unimmunized subpopulations such as ethnic minorities. A serologic survey among a Gypsy
community in Italy found that despite only 26% documented immunization coverage, serum neu-
tralizing antibodies to poliovirus types 1, 2, and 3 were detected in 81%, 94%, and 63% of the 86
persons studied. While the high level of immunity found in this community may have been due to

Downloaded from http://jid.oxfordjournals.org/ at Istituto Superiore di Sanita on August 21, 2012

secondary spread of vaccine virus, the possibility of unrecognized circulation of wild polioviruses
cannot be excluded. Targeted immunization of such groups may be the most efficient means of
eliminating the risk of importation-associated outbreaks.

Although indigenous wild polioviruses have been eliminated
from western Europe for several years, unimmunized subpopu-
lations will continue to present a risk of importation-associated
outbreaks until such time as the global goal of polio eradication
is achieved [1, 2]. In many European countries, Gypsies are at
a particular risk of reintroducing wild polioviruses because of
their low immunization coverage, ongoing contact with areas
in which polio is endemic, and often nomadic lifestyles [3].
In November 1994, a case of acute flaccid paralysis in a 13-
month-old Gypsy child from Rome was tentatively diagnosed
as poliomyelitis on the basis of clinical and electromyographic
findings. Although virologic studies did not detect evidence of
a poliovirus infection, the case provided a rare opportunity to
evaluate the risk of sustained poliovirus transmission in a
Gypsy community and the potential for spread to the general
population.
Background
The last case of poliomyelitis in Italy due to indigenous wild
poliovirus was in a patient who developed paralysis in 1982 [4].
Since 1980, 6 cases of vaccine-associated poliomyelitis and 3 im-
ported cases, from Iran, India, and Libya, have been reported [4].
Immunization coverage with at least three doses of oral polio
vaccine (OPV) was 95% for children <5 years old in the general
Italian population in 1994 (Ministry of Health, Italy).
Informed consent was obtained from each person that participated in this
trial or his or her guardian.
Financial support: Istituto Superiore di Sanita (Prevention of Risk Factors
in Maternal and Child Health, project no. Art.12 D.L.502/92-research line
4.4 "Surveillance of Acute Flaccid Paralysis in Italy").
Reprints or correspondence: Dr. Francesco Forastiere, Osservatorio Epide-
miologico, Regione Lazio, Via di Santa Costanza, 53, 00198 Rome, Italy.
The Journal of Infectious Diseases 1997; 175(Suppl 1}:S86-8
© 1997 by The University of Chicago. All rights reserved.
0022-1899/97/75S1-0016$01.00
The Gypsy community from which the suspected polio case was
notified in November 1994 consisted of 26 families living in a
collection of recreational vehicles. Sewage facilities were shared,
and water for drinking and bathing was taken from a communal
tap. The case prompted the community to work with public health
authorities to determine their risk of vaccine-preventable diseases
and update their immunization status.
Methods
A standardized questionnaire was used to collect demographic
data, vaccination histories, travel details, and contacts with coun-
tries in which polio is endemic from all members of the Gypsy
camp from which the case was notified. The reported immunization
status of each person was corroborated by reviewing immunization
cards and local health unit records. The immunization status of
each person was then classified as documented (written record),
reported (no written record but verbally reported), no history (nei-
ther written nor verbal), or unknown (no written record and re-
ported as unknown). For those with no immunization history, the
number of contact doses to which they may have been exposed
was estimated by calculating the number of doses given to other
family members.
Serum samples were collected from all consenting persons. An-
tibody titers to poliovirus types 1, 2, and 3 were determined by a
standard microneutralization assay in Hep-2 cells [5]. Briefly, 2-
fold dilutions ofsera were challenged with 100 TCID so of reference
strains of poliovirus types 1-3 (Mahoney, MEF-l, and Leon, re-
spectively). Neutralization mixtures were inoculated onto cell
monolayers, and cytopathic effect was scored daily for 3- 5 days.
Serum neutralizing antibody titers were expressed as the reciprocal
of the highest dilution shown to completely inhibit cytopathic
effect. Titers were considered positive at ;:,: 1:8 dilution. Anti-teta-
nus and -diphtheria antibody titers were measured as a direct con-
trol of the reported immunization status. Titers were determined
with an indirect hemagglutination test using turkey erythrocytes
sensitized with tetanus toxoid or diphtheria toxoid (30 Lf U/mL).
Reference standards were established by serum neutralization us-
ing human IgG containing 150 IU/mL tetanus toxoid or 10 lUI
JID 1997;175 (Suppll) Gypsy Populations and Polio Eradication S87

Table 1. Comparison of selected characteristics of the total Gypsy immunization with OPV was documented for 22 (26%), ver-
community and the subgroup with serologic results available, Rome, bally reported for 19 (22%), and unknown for 14 (16%).
1994.
Thirty-one (36%) had no history of OPV immunization. Of
Subgroup with those with documented immunization, 21 had received at
Total serologic least three doses ofOPV; of the 21 with documented tetanus
Variable population results p* and diphtheria immunization, 5 had received three or more
doses of diphtheria-tetanus vaccine.
Total 149 86
There was no significant difference in the presence of
Sex
Male 83 44 .5 serum neutralizing antibody to poliovirus type 2 by immuni-
Female 66 42 zation status; 100%, 95%, and 91% of persons with docu-
Age group, years mented, reported, and no history or unknown immunization
<1 1 0 .49 were seropositive, respectively (P = .342). Of the persons
1-4 19 8
28 15
with documented OPV immunization, 100% and 77% were
5-9
seropositive for poliovirus types 1 and 3, respectively, while

Downloaded from http://jid.oxfordjournals.org/ at Istituto Superiore di Sanita on August 21, 2012

10-14 28 21
>14 73 42 79% and 37% of those with a reported immunization history
Presence in camp were seropositive. Among those with no immunization his-
<1 year 46 28 .59 tory or unknown status, 73% and 67% had anti-poliovirus
1-5 years 34 22
type 1 and -type 3 antibodies, respectively. A similar pattern
6-10 years 42 23
Since birth 26 13 was seen when the analysis was restricted to children < 10
Missing 1 0 years old (table 2). In contrast to the findings for poliovirus
Previous place of residence t antibodies, only 3 persons, all of whom had a documented
Rome 22 19 history of immunization and were ;::10 years of age, were
Italy (excluding Rome) 72 42 .08
seropositive for tetanus; no persons were seropositive for
Europe (excluding Italy) 27 10
Missing 2 2
diphtheria.
Among the 31 persons with no history of immunization, the
NOTE. Data are no. of subjects. probability of being seropositive to poliovirus type 1, 2, or 3
* X 2• increased with age (data not shown). The subgroup of 14 with
t Excluding people born at the camp.
documented exposure to contact doses showed a significant
correlation between age and the number of doses to which a
person was exposed (r = .70; 95% confidence interval, 0.27-
mL diphtheria toxoid. The minimum titer that was considered
0.90). Age-adjusted geometric mean antibody titers were high-
protective was 0.01 IU/rnL.
est among unimmunized persons who were exposed to immu-
Univariate statistics (X 2, Fisher's exact test) were used to com-
pare the characteristics of the total population and the subgroup nized family members (table 3).
for which serologywas available. Differences in the proportion of Discussion
persons who seroconverted by immunization status category were
evaluated with X2 • Linear regression was used to test for associa- Although the documented OPV immunization coverage in
tions between age and the number of contact doses. Logistic and this Gypsy community is well below the Italian average (26%
linear regression models were constructed to control for age while
assessing the effect of contact doses on serologic status and the
Table 2. Prevalence of poliovirus antibodies by immunization status
geometric mean titer of anti-poliovirus antibodies. and age group, Gypsy community, Rome, 1994.

Immunization status
Results
No history
The Gypsy community we studied consisted of 149 per- Age group Antibody type Documented Reported or unknown P"
sons, 86 (58%) of whom provided blood samples. There
were no significant differences in sex, age, time in the com- < 10 years No. of subjects 8 4 11
Poliovirus 1 100.0 50.0 45.5 .018
munity, or place of last residence between those who did
Poliovirus 2 100.0 100.0 81.8 .162
and did not provide samples (table 1). Of the 47 who were Poliovirus 3 75.0 25.0 27.3 .05
not Italian nationals, 33 were from the former Yugoslavia ~ 10 years No. of subjects 14 15 34
and 14 were from France; all had been in Italy for >5 years Poliovirus 1 100.0 86.7 82.4 .11
except for 10 who had arrived from France in the previous Poliovirus 2 100.0 93.3 94.1 .45
Poliovirus 3 78.6 40.0 79.4 .50
6-12 months. Recent contacts with countries in eastern Eu-
rope in which polio is endemic could not be excluded. Of NOTE. Antibody data are %.
the 86 persons for whom serology results were available, * X 2 for trend.
S88
Table 3. Age-adjusted poliovirus antibody titers for unimmunized
subjects with and without documented exposure to immunized family
members, Gypsy community, Rome, 1994.
Antibody geometric mean
titer
Age-
Poliovirus Exposed Unexposed adjusted
type (n = 14) (n = 14) difference *
1 45.1 28.1 25.6
2 94.3 39.0 68.7
3 15.8 11.8 7.9
* From multiple linear regression analysis.
vs. 95%), >94% of the persons studied were found to have
serum neutralizing antibodies to poliovirus type 2, while 81%
and 63% were seropositive for types 1 and 3, respectively. A
number of factors suggest that secondary spread of vaccine
virus may have contributed to the high level of antibodies seen
among the unimmunized Gypsies: Wild poliovirus type 2 has
not circulated in Europe for several years, geometric mean
antibody titers were highest among unimmunized persons who
were exposed to immunized family members, and the propor-
tion of unimmunized children with antibodies to poliovirus
types 1, 2, and 3 is consistent with the pattern expected with
secondary spread [6]. Because poliovirus transmission is pre-
dominantly fecal-oral, the spread of either vaccine or wild
poliovirus could have been facilitated by the poor hygienic
conditions under which this Gypsy community lived.
While indigenous poliovirus transmission was interrupted in
Italy by 1983 [4], the possibility of unrecognized exposure of
this Gypsy community to imported wild polioviruses cannot be
excluded, as there has been a significant potential for ongoing
contact with persons from countries in which polio is endemic,
particularly Balkan countries. Although acutely paralyzed chil-
dren rapidly receive medical care in Italy, the very high ratio of
wild poliovirus infection to paralysis could result in substantial
silent transmission before a case of paralysis occurred [2].
The number of persons who had received OPV could have
been underestimated in this study because of incomplete data,
but this is doubtful, as the community is served by a single
health unit that maintains individual immunization histories
and records of immunization activities. Furthermore, the lack
of antibodies to tetanus or diphtheria among those with no
documented immunization indicates that the immunization sta-
tus data are relatively accurate. Although the sample size in
this study is relatively small and involves only one Gypsy
community, the results may be representative of other commu-
View publication stats
Aylward et al. JID 1997; 175 (Suppl 1)
nities because of similarities in their immunization status, living
conditions, and travel histories.
Despite the relatively high level of immunity seen in this
study, an importation of wild poliovirus into this Gypsy popula-
tion could still result in substantial morbidity. These findings
reinforce the need for targeted immunization activities similar
to the' 'mopping up" that is recommended by the World Health
p*
Organization [2] to eliminate the last pockets of polio-suscepti-
.24 ble persons. As part of the response to the suspected polio case
.04 identified in this Gypsy community, the immunization status
.21 of its members was reviewed and updated by the local health
unit. Other health units in the Rome area are also conducting
catch-up immunization among their Gypsy populations and
developing a plan for ensuring the ongoing immunization of
Downloaded from http://jid.oxfordjournals.org/ at Istituto Superiore di Sanita on August 21, 2012
these groups. Similar activities have previously been successful
in boosting the immunization status of itinerant populations in
other European countries [7].
Eventually, national certification of polio eradication will
require evidence that high-risk populations such as these unim-
munized Gypsies and other ethnic minorities have sufficient
immunization coverage to prevent the importation and spread
of wild polioviruses [8].
The findings of this study support the proposition that sec-
ondary spread of vaccine virus may reduce the potential for
polio outbreaks in high-risk populations with relatively low
immunization rates. However, additional targeted immuniza-
tion activities are required to eliminate the potential for sus-
tained wild poliovirus transmission in such groups and the
possibility of spread into the general population.
References
1. Oostovogel PM, van Wijngaarden JK, van der Avoort HGAM, et al. Polio-
myelitis outbreak in an unvaccinated community in the Netherlands,
1992-3. Lancet 1994;344:665-70.
2. Hull HF, Ward NA, Hull BP, Milstien JB, de Quadros e. Paralyticpoliomyeli-
tis: seasoned strategies, disappearing disease. Lancet 1994;343:1331-7.
3. Expanded Programme on Immunization. Status of poliomyelitis eradication
in the WHO European Region. Wkly Epidemiol Rec 1994; 69:281-4.
4. Novello F, Lombardi F, Amato C, et al. Paralytic poliomyelitis in Italy
(1981-1985). Eur J EpidemiolI987;3:54-60.
5. Oberhofer TR, Brown GC, Monto AS. Seroimmunity to poliomyelitis in
an American community. Am J Epidemiol 1975; 101:333-9.
6. Chen R, Hanfling M, Hausinger S, et al. Extent of secondary spread of oral
polio vaccine virus in inner-city preschool children [abstract 1403]. In:
Program and abstracts of the 32nd Interscience Conference on Antimicro-
bial Agents and Chemotherapy (Anaheim, CA). Washington, DC: Ameri-
can Society for Microbiology, 1992:344.
7. Bell EJ, Riding MH, Collier PW, Wilson NC, Reid D. Susceptibility of
itinerants ("travelling people") in Scotland to poliomyelitis. Bull World
Health Organ 1983;61:839-43.
8. Robbins Fe. Eradication of polio in the Americas. JAMA 1993;270:1857-9.