862
Outbreak of Paralytic Poliomyelitis in a Highly Immunized Population in Jordan
Mary R. Reichler, Adnan Abbas,* Sa'ad Kharabsheh,
Azmi Mahafzah, James P. Alexander, Jr., Philip Rhodes,
Samir Faouri, Haider Otoum, Samir Bloch,
Mazen Abdel Majid, Mick Mulders, Rafi Aslanian,
Harry F. Hull, Mark A. Pallansch,
and Peter A. Patriarca*
Polio Eradication Activity and Data Management Branch, National
Immunization Program, and Enterovirus Branch, National Center for
Infectious Diseases, Centers for Disease Control and Prevention,
Atlanta, Georgia; Disease Prevention and Control Directorate and
Jordan Vaccine Institute, Ministry of Health, Department of Laboratory
Medicine, Jordan University Hospital, and Department of Pediatrics, AlBashir Hospital, Amman, Jordan; Laboratory of Virology, National
Institute for Public Health and Environmental Protection (RIVM),
Bilthoven, Netherlands; Elimination and Eradication ofDiseases,
Eastern Mediterranean Regional Office, World Health Organization,
Alexandria, Egypt; Global Programme for Vaccines and Immunization,
World Health Organization, Geneva, Switzerland
Between November 1991 and March 1992, 37 cases of paralytic poliomyelitis occurred in Jordan,
where none had been reported since 1988. Of these, 17 (50%) of 34 patients had received at least
three doses of oral poliovirus vaccine (OPV3). The first and 2 subsequent case-patients were children
of Pakistani migrant workers, and the first 8 and a total of 27 (75%) case-patients resided in or
near the Jordan Valley. A seroepidemiologic study of 987 children in all regions of Jordan was
performed to assess OPV3 coverage and immune response to OPV. Although OPV3 coverage by 12
months of age was high (96%) in the general population, coverage was lower among Pakistani
(21%), Bedouin (63%), and Gypsy (9%) children (P < .001). Seroprevalences for poliovirus type 3
were 71% in the Jordan Valley versus 81% in other regions after 3 doses of OPV (P < .06) and
77% in the Jordan Valley versus 98% in other regions after 5 doses of OPV (P < .001). This outbreak
demonstrates the importance of achieving high seroimmunity to infection in all geographic areas
to prevent the reintroduction and spread of imported strains of wild poliovirus.
Paralytic poliomyelitis was rapidly eliminated from industrialized countries and its incidence markedly reduced worldwide
once high coverage with at least three doses of the live attenuated oral poliovirus vaccine (OPV) was achieved [1, 2]. Despite
high coverage with OPV, some countries experience outbreaks
of paralytic poliomyelitis caused by imported strains of wild
poliovirus several years after indigenous wild poliovirus transmission has ceased [3-5]. Strategies to prevent the reintroduction and spread of wild poliovirus in polio-free areas are essential to achieve the goal of global eradication of paralytic
poliomyelitis, planned for the year 2000.
We report the results of our investigation of an unusual
epidemic of paralytic poliomyelitis in Jordan, a country with
high OPV coverage and no reported poliomyelitis cases for
Presented in part: 32nd Interscience Conference on Antimicrobial Agents
and Chemotherapy, Anaheim, California, October 1992 (abstract 1723); 34th
Interscience Conference on Antimicrobial Agents and Chemotherapy, Orlando,
Florida, October 1994 (abstracts J93 and J95).
Informed consent was obtained from the parents of children enrolled in
these studies.
Reprints or correspondence: Dr. Mary R. Reichler, Mailstop E-05, NIP,
CDC, 1600 Clifton Rd., Atlanta, GA 30333.
* Present affiliations: Department of Community Medicine, Jordan University, Amman, Jordan (A.A.); Center for Biologics Evaluation and Research,
Food and Drug Administration, Bethesda, Maryland (P.P.).
The Journal of Infectious Diseases 1997; 175(8uppl 1):862-70
© 1997 by The University of Chicago. All rights reserved.
0022-1899/97/7581-0012$01.00
> 3 years. The epidemic occurred during the winter (the low
season for wild poliovirus transmission) and remained localized
to one region of the country for several months. Large outbreaks ofparalytic poliomyelitis are infrequent in highly immunized populations, generally occur during the summer months,
and are usually associated with rapid and wide geographic
spread.
In this report, we examine the relationship of unimmunized
subpopulations, regional differences in immune response to
vaccine, vaccination timing, and other factors to the risk of
epidemic paralytic poliomyelitis in a population with high overall vaccination coverage.
Background
Children in Jordan receive doses of OPV at 3, 4, 5-6, and
18 months of age. Estimated vaccination coverage with three
doses of OPV (OPV3) by 1 year of age in Jordan has been
> 85% since 1986 and was estimated in 1990 by cluster survey
methodology to be 92%. Prior to the current outbreak, no cases
of poliomyelitis had been reported in Jordan since mid-1988.
Although Jordanians comprise >95% ofthe total population
in all areas of Jordan, there are a number of distinct subpopulations: (1) migratory Bedouin tribes, found throughout Jordan;
(2) migratory agricultural workers from Pakistan, residing in
the southern Jordan Valley (October-April) and rural areas of
Amman governorate (May-September); and (3) Gypsies, living in and near the Jordan Valley (October-April) and in north-
JID 1997; 175 (Suppl 1)
Polio Outbreak in Jordan
em Jordan (May-September). In addition, during the 1991
Gulf War ....... 500,000 non-Jordanians sought temporary refuge
in Jordan and ....... 300,000 Jordanians living in Kuwait returned
to Jordan and were resettled throughout the country.
Methods
Case ascertainment. All hospitals and health centers in Jordan
were informed about the outbreak:and instructed to report all cases
of acute flaccid paralysis (whether or not acute poliomyelitis was
suspected) to the Jordan Ministry of Health. All cases were investigated by an expert team and confirmed or discarded according to
standard World Health Organization criteria [6].
Virology. Stool specimens from 16 case-patients were processed at the Jordan Vaccine Institute in Amman and the National
Institute for Public Health and Environmental Protection in Bilthoven, Netherlands. Enteroviruses were isolated and identified as
polioviruses or nonpolio enteroviruses, and intratypic differentiation was performed on poliovirus isolates using previously described techniques [7]. To determine the origin of the type 1 wild
polioviruses linked to the Jordan outbreak, we performed partial
genomic sequencing of 8 of 9 outbreak strains and compared data
from these strains with a database containing nucleotide sequences
of >200 type 1 wild polioviruses isolated between 1975 and 1992
from the Middle East, Africa, Asia, North America, and South
America, using previously described techniques [3, 8-10].
Seroepidemiologic studies. To evaluate the geographic extent
of spread of wild poliovirus during the outbreak and to determine
the immune state of children in different regions of Jordan, we
obtained sera from the following groups of children in the fourth
month of the outbreak (February 1992), prior to the first nationwide
mass campaign: (1) 428 control children from 12 towns in the
Jordan Valley (the region with the highest paralytic attack rate),
including children from 6 towns with and 6 towns without detected
cases; (2) 43 control children from Safi (located in the Gore Valley
[40 kilometers south of the Jordan Valley], where no cases were
detected); (3) 203 control children from the 8 governorates in
Jordan (Amman, n = 71; Irbid, n = 43; Zarka, n = 39; Balka, n
= 14; Mafraq, n = 11; Karak, n = 9; Tafila, n = 9; and Ma'an,
n = 7), excluding Jordan Valley districts; (4) 102 Pakistani (n =
62), Bedouin (n = 18), and Gypsy (n = 22) children living in or
near the Jordan Valley; and (5) 17 case-patients ~ 21 days after
paralysis onset (11 who had received three or more doses of OPV
[fully immunized] and 6 who had received no OPV doses [unimmunized] or one to two OPV doses [partially immunized] at least
21 days prior to paralysis onset) (figure 1). Since exposure to wild
poliovirus type 1 had already occurred in parts of Jordan, we
measured antibody to poliovirus type 3 to assess immune response
to OPV at the time of the outbreak.
To examine the immune state of children in different regions
of Jordan following two nationwide mass campaigns, we obtained
sera 6 weeks after the second campaign (May 1992) from 198
control children from all 8 governorates in Jordan, all of whom
had received both mass campaign doses of OPV.
To determine the immune state of children in different regions
of Jordan at baseline (in the absence of wild poliovirus circulation),
we obtained sera in December 1993 and January 1994 from the
following groups of children born after the outbreak: (1) 74 control
S63
children from 2 towns in the Jordan Valley (38 from Abu-Obeideh
and 36 from Almashara); (2) 45 control children from Safi; (3) 40
control children from Amman governorate; and (4) 40 control
children from Zarka governorate (figure 1).
All control children from towns in the Jordan Valley and Safi
were a convenience sample selected according to a history (documented by vaccination card) of having received three or more
doses of OPV at least 21 days prior to serum collection and age
12-24 months at the time of serum collection. All control children
from Jordan governorates were a cluster survey sample selected
according to a history (documented by vaccination card) of having
received three OPV doses through the routine program at least 30
days prior to serum collection and age 7-12 months at the time of
serum collection. Pakistani, Bedouin, and Gypsy control children
represented all children 7- 36 months of age in these subpopulations that could be identified in or near the Jordan Valley at the
time the survey was conducted.
All 987 sera from case-patients and control children enrolled in
the seroepidemiologic studies were tested in triplicate with a modified microneutralization technique at the Centers for Disease Control and Prevention (CDC), in dilutions ranging from 1/8 to 11
1024 [7].
Immunization coverage studies. Written, standardized questionnaires providing immunization information (documented by
vaccination card) were completed at the time sera were collected
for all 987 children enrolled in the seroepidemiologic studies.
Evaluation of the cold chain. During the outbreak (January
and February 1992), 11 vaccination sites (the central store at the
Jordan Vaccine Institute in Amman and 10 peripheral sites in the
JordanValley) were visited to observe vaccine storage, handling,
and administration techniques and to review cold-chain maintenance records.
Vaccine efficacy. Using a standard formula [11], we estimated
the efficacy of three or more doses of OPV administeredthroughthe
routineprogram among childrenin Jordan at the time of the outbreak.
Statistical analysis. Statistically significant differences in
type-specific antibody titers and vaccination timing among the
various groups of children were assessed with a nonparametric
test (Wilcoxon rank sum test) using SAS (Cary, NC) software.
Results
Outbreak. Between November 1991 and March 1992, 37
cases of paralytic poliomyelitis occurred in Jordan (figure 2).
Of these patients, 33 (89%) were <36 months of age (range,
1-108) and 17 (50%) had received at least three doses ofOPV;
5 (14%) case-patients died. Type 1 wild poliovirus was isolated
from 9 (56%) of 16 case-patient stool specimens. The first 8
and a total of 27 (75%) cases occurred in the Jordan Valley (n
= 18) or neighboring districts (n = 9) (figure 2). Paralytic
attack rates were 13/105 in the Jordan Valley and 0.5/10 5 outside the Jordan Valley. Although 33 (92%) case-patients were
Jordanian, the first and 2 subsequent case-patients were children of Pakistani migrant workers. In the Jordan Valley, paralytic attack rates were 111105 among Jordanians and 86/10 5
among Pakistanis.
S64
Reichler et al.
JID 1997; 175 (Suppl 1)
LakeTiberias
o
e
Bodies of water
Jordan Valley and
Gore Valley
• Study sites
Gore Valley
o
o
"
25 Km
I
I
I
I
i
,
25
50 Miles
Gulf of
Aqaba
Figure 1.
Map of Jordan showing all 8 Jordan governorates and seroepidemiologic study sites in Jordan Valley and Gore Valley.
A door-to-door vaccination campaign targeting all children <5 years of age with OPV was conducted in the Jordan
Valley between 29 January and 6 February 1992; estimated
vaccination coverage was 95%. Since cases continued to
occur in February, two nationwide mass vaccination campaigns were conducted, the first from 24 February to 2 March
and the second from 6 to 13 April; estimated coverage for
both nationwide campaigns was >95%. Although 4 cases
occurred in the 3-week period following the first nationwide
vaccination campaign, none occurred following the second
campaign (figure 2). No further laboratory-confirmed cases
of poliomyelitis have been reported in Jordan through mid1996.
Virology. Type 1 wild poliovirus was isolated from 9
(56%) of 16 case-patient stool specimens. All 8 outbreak isolates analyzed by partial genomic sequencing were closely related to one another (98% similarity of the VP1I2A region),
suggesting a recent common origin. The Jordan isolates were
genotypically distinct from prior wild type 1 polioviruses from
Israel (1988, 75% similarity) and most other countries in the
Middle East but matched isolates from the 1988-1989 outbreak
in Oman (95% similarity) and a 1992 isolate from Pakistan
(98% similarity) [9, 10].
Geographic extent ofspread of wild poliovirus during the outbreak. Vaccinated and unvaccinated case-patients, control children from towns in the Jordan Valley with and without cases,
Pakistani control children, and Bedouin control children who had
blood samples drawn during the outbreak all had similar type 1
neutralizing antibody profiles, suggesting that widespread exposure to wild poliovirustype 1 occurred in the Jordan Valley during
the outbreak (figure 3). Although seroprevalences to poliovirus
type 1 were similar for Jordan Valley controls and non-Jordan
Valley governoratecontrols who had blood samples drawn during
the outbreak (94% and 97%, respectively),titerswere significantly
higher among Jordan Valley controls (geometric mean titers of
898 vs. 616 [P < .05], respectively), suggesting that exposure to
wild poliovirus was greater inside than outside the Jordan Valley
(figure 3).
Polio Outbreak in Jordan
JID 1997;175 (Supp11)
S65
6.----------------------------,
N=37
5
4
(I)
<V
-
D Outside Jordan Valley
-
ffiilll Near Jordan Valley
•
(I)
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In Jordan Valley
«S
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<V
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:::J
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1
~
r-- -
r--
... ..
I
Oct
Nov
1991
Dec
Jan
Time (Weeks)
Feb
I
I
I
March
April
1992
Figure 2. Cases of paralytic poliomyelitis in Jordan by geographic region and week of onset. Of 37 cases, first 8 and total of 27 (75%)
occurred in Jordan Valley (N; n = 18) or neighboring districts (n = 9). Arrows indicate timing of 4 mass vaccination campaigns, 2 limited
to Jordan Valley and 2 conducted nationwide. Whereas cases continued to occur following first Jordan Valley mass vaccination campaign,
very few cases occurred following first nationwide campaign.
Figure 4 presents the neutralizing antibody profiles for children in selected towns inside and outside the Jordan Valley
who had blood samples drawn during (figure 4A) versus after
(figure 4B) the outbreak. Titers were significantly lower in
Jordan Valley controls who were born and had blood samples
drawn after the outbreak than in those who had blood samples
drawn during the outbreak. Titers were also consistently lower
among controls outside the Jordan Valley who were born and
had blood samples drawn after the outbreak compared with
those who had blood samples drawn during the outbreak, suggesting that wild poliovirus type 1 had already spread to at
least some areas outside the Jordan Valley prior to the first
nationwide mass campaign.
Immune state of children in different regions of Jordan.
As illustrated in figure 5, the immune response to OPV was
consistently lower among control children in the Jordan Valley
than among those in other regions of Jordan. Seroprevalence
rates after three doses of OPV for poliovirus type 3 were 71%
in the Jordan Valley versus 81% (range, 64%-100%) among
governorate controls in other regions (P < .06). Seroprevalence
rates after five doses of OPV for poliovirus type 3 were 77%
in the Jordan Valley versus 98% (range, 92%-100%) in other
regions (P < .001). Regions with higher paralytic attack rates
were more likely to have lower seroprevalence rates for poliovirus type 3 after three and five doses of OPV (figure 5). In
addition, the increase in seroprevalence rates after five versus
three doses of OPV for poliovirus type 3 was significantly
smaller in the Jordan Valley compared with other regions (6%
vs. 17%, respectively; P < .001).
Immunization coverage studies. There was no association between paralytic attack rate and OPV vaccination coverage, which
ranged from 96% to 100% by region. Although survey children
in the general population in the Jordan Valley were selected on
the basis of having received at least three doses of OPV, this is
unlikely to represent a significant bias toward higher coverage
estimates in this region, since very few partially immunized or
unimmunized children were identified during the survey.
Figure 6 presents the timing of OPV receipt among controls
in the general population and Pakistani, Gypsy, and Bedouin
subpopulations in the Jordan Valley. Although OPV3 coverage
by 12 months of age was high among children in the general
population residing in the Jordan Valley (96%), coverage was
lower among Pakistani (21%), Bedouin (63%), and Gypsy (9%)
children (P < .001, comparing general population and Pakistani
children, general population and Bedouin children, and general
population and Gypsy children). Delays in completing OPV3
occurred in all groups in the Jordan Valley surveyed: Only 71%
of general population, 37% of Bedouin, 3% of Pakistani, and no
Gypsy children had received OPV3 on schedule, by 6 months of
age (figure 6). Although coverage at 12 months of age was similar
for children in the general population residing inside and outside
the Jordan Valley (96% vs. 100%, respectively), vaccination de-
S66
lID 1997; 175 (Suppl 1)
Reichler et al.
7
6
30
Cases
(n=17)
25
Pakistani
(n=62)
5
20
4
15
3
10
2
5
<8
120
100
o
8
8
Inside Jordan Valley
townswith cases
<8
8
16
32
64
128
256
512
1024 >1024
16
32
64
128
256
512
1024 >1024
Bedouin
(n=18)
(n=217)
6
80
4
60
40
<8
120
100
8
16
32
64
128
256
512
<8
1024 >1024
80
Inside Jordan Valley
towns without cases
8
Outside Jordan Valley
(n=203)
(n=211)
60
80
60
40
40
20
20
o
<8
8
16
32
64
128
256
512
1024 >1024
<8
8
16
32
64
128
256
512
1024 >1024
Titer
II~Opv
o
<30PV
Figure 3. Seroprevalence of neutralizing antibody to poliovirus type 1 among case-patients and controls during 1991-1992 outbreak of type
1 paralytic poliomyelitis in Jordan. Vaccinated and unvaccinated case-patients, control children inside and outside Jordan Valley, and Pakistani
and Bedouin control children who had blood samples drawn during outbreak all had similar type 1 neutralizing antibody profiles.
lays were significantly greater among children inside the Jordan
Valley (71% inside vs. 87% outside had received OPV3 by 6
months of age; P < .001) (data not shown). Regions in Jordan
with higher paralytic attack rates tended to have greater delays in
completing OPV3 (data not shown)
Evaluation of the cold chain. No abnormalities in vaccine
storage or handling were noted in the central store in Amman
or in peripheral sites in the Jordan Valley.
Vaccine efficacy. Vaccine efficacy was estimated to be
96% overall in Jordan, with separate estimates of 94% inside
and 98% outside the Jordan Valley.
Discussion
The 1991-1992 poliomyelitis outbreak in Jordan occurred
following importation of wild poliovirus into an area that had
20
15
20
Almashara A
(n=34)
15
10
10
5
5
0
8
<8
16
32
64
128
256
512
1024
>1024
25
20
...
...,
867
Polio Outbreakin Jordan
JID 1997;175 (Suppll)
0
Almashara B
(n=36)
<8
8
64
128
256
512
32
64
128
256
512
16
32
64
128
256
512
18
32
64
128
256
512
64
128
16
32
1024
>1024
1024
>1024
25
Abu Obeideh A
(n=34)
20
15
15
10
10
5
5
Abu Obeideh B
(n=38)
CD
;;
.c
...,
.~
0
<8
8
16
32
64
128
256
512
1024
>1024
25
0
Amman A
(n=71)
25
tn
(5
20
20
15
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C
10
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5
...
...,
0
....0
.
0
Z
0
<8
8
16
32
64
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256
512
1024
>1024
0
Zarka A
(n=39)
15
10
5
5
<8
8
16
32
35
30
25
64
128
256
512
1024
>1024
Amman B
(n=40)
<8
8
0
Zarka B
(n=40)
<8
8
35
Safi A
(n=43)
30
25
20
20
15
15
10
10
5
5
0
16
20
10
0
8
5
20
15
<8
30
30
<8
8
16
32
0
Safi B
(n=45)
<8
8
18
Titer
Figure 4. Seroprevalence of neutralizing antibody to poliovirus type 1 among controls from selected towns inside and outside Jordan Valley
who had blood samples drawn during (A) vs. those who were born and had blood samples drawn after (B) 1991-1992 outbreak of type 1
paralytic poliomyelitis. Titers were consistently lower among controls inside and outside Jordan Valley who were born and had blood samples
drawn after outbreak compared with those who had blood samples drawn during outbreak.
S68
Reichler et al.
100
..........
90
70
CI)
>
:.p
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120
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.. . . . -.-.... .-..••••
~
80
JID 1997;175 (Suppll)
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60
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lo-
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30
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LO
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0
a.
(I)
l0-
'------r---r---..---~-''3-~
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.....- - -....LJ~------­
3 doses of OPV •••••••
o
s
-........
CI)
10
0:::
0
5 doses of OPV - -
Figure 5. Proportion of children with neutralizing antibodies to poliovirus type 3 after 3 and 5 doses of oral poliovirus vaccine (OPY) and
attack rates of paralytic poliomyelitis by region in Jordan. Seroprevalence rates after 3 doses of OPY for poliovirus type 3 were 71% in Jordan
Valley vs. 81% (range, 64%-100%) among controls in other regions (P < .06). Seroprevalence rates after 5 doses of OPV for poliovirus type
3 were 77% in Jordan Valley vs. 98% (range, 92%-100%) in other regions (P < .001). Statistical comparisons were made with Wilcoxon
rank sum tests using SAS (Cary, NC) software.
been polio-free for several years. A gradual build-up of susceptibles likely occurs even in a highly immunized population
once endemic wild poliovirus transmission has ceased. Despite
this, outbreaks rarely occur if high levels of vaccination coverage are maintained. Our investigation identified several factors
that greatly increased the number of susceptibles in the Jordan
Valley, thus contributing to the outbreak.
While coverage with at least three doses of OPV was very
high among children in the general population in all areas of
Jordan at the time of the outbreak, there were 3 separate migratory subpopulations in the Jordan Valley whose vaccination
levels were considerably lower: children of Pakistani migrant
workers, Gypsies, and Bedouins. The initial case in the outbreak occurred in a Pakistani child, and the attack rate in this
subpopulation was 8-fold higher than among children in the
general population in the Jordan Valley. The potential for wild
poliovirus transmission to be sustained within pockets of unvaccinated children with subsequent spread to fully vaccinated
children is well established [12, 13]. Thus, the introduction
and spread of wild poliovirus by unimmunized migratory
groups likely contributed to infection in the highly immunized
general population in Jordan. Although coverage with at least
three doses of OPV by 12 months of age was high, fewer
than three-quarters of children in the general population in the
Jordan Valley had received these doses on schedule, by 6
months of age. Furthermore, even greater delays in receipt of
OPV doses occurred for Pakistani, Gypsy, and Bedouin children. Thus, delays in completing the OPV schedule among
children in the Jordan Valley substantially increased the pool
of unvaccinated children susceptible to poliovirus infection,
likely increasing transmission. Achieving high coverage with
at least three doses of OPV in a timely fashion is important to
provide sufficient population immunity to stop transmission if
reintroduction of wild poliovirus occurs.
Regional differences in antibody responses to OPV were
present in Jordan at the time of the outbreak despite high
coverage with three doses of OPV in all regions. In the Jordan
Valley, seroprevalence rates to poliovirus type 3 after three
and five doses of OPV were significantly lower than in other
regions of the country. Thus, suboptimal immune response to
as many as five doses of OPV among children in the general
population in the Jordan Valley produced a gap in immunity
that also contributed to spread of an imported wild poliovirus
strain during the outbreak. Regional variation in immune response to OPV has also been noted in Oman, where outbreaks
due to imported strains of wild poliovirus have been a recurrent
problem [3, 14].
Although risk factors for suboptimal immune response to
OPV could not be evaluated in the current study, factors associated with low seroprevalence in other studies include residence
in tropical and subtropical areas; low socioeconomic status;
and diarrhea, nonpolio enterovirus infection, or other enteric
JID 1997;175 (Suppl 1)
Polio Outbreakin Jordan
S69
100 , . - - - - - - - - - - - - - -
80
CI)
Q
Figure 6. Cumulative coverage with at
least 3 doses of oral poliovirus vaccine
(OPV3) by month of age among controls in
general population and Pakistani, Gypsy, and
Bedouin subpopulations in Jordan Valley. Although OPV3 coverage by 12 months of age
was high among Jordanian children, coverage
was lower among Pakistani, Bedouin, and
gypsy children. Delays in completing OPV3
occurred in all groups surveyed.
!
~
o
o
60
e
..
~
40
CI)
0.
20
0"'--.......-
o
.......- - - - - - - -..........-....
2
3
4
567
8
9
10
11
12
Age (months)
Jordanian Bedouin Pakistani Gypsy
infections at the time OPV is administered [15-18]. At the
time of the Jordan outbreak, the socioeconomic status among
residents of the Jordan Valley was generally considerably lower
than in most other areas of Jordan. Crowding and poor sanitation, associated with rapid spread of poliovirus and other enteric pathogens, were present in a number of areas in the Jordan
Valley. Furthermore, the Jordan Valley is one of only two areas
in Jordan with a subtropical rather than an arid or temperate
climate. Thus, many of the risk factors for suboptimal immune
response to OPV identified in other settings were present in
the Jordan Valley at the time of the outbreak.
The Jordan outbreak was associated with a 20-fold higher
paralytic attack rate in the Jordan Valley than in other regions
of the country. Our investigation findings suggest that at least
three factors-the presence of unimmunized subpopulations,
delays in receipt of OPV, and lower immune response to OPV
in the Jordan Valley compared with other regions of the country-likely contributed to the high attack rate in that region.
In addition, the seasonal migration of all three underimmunized
subpopulations (Pakistanis, Bedouins, and Gypsies) to the Jordan Valley in the month prior to the outbreak may have been
associated with the initial introduction and spread of wild poliovirus in that region. Furthermore, geographic and climatic factors-a steep mountain range separating the Jordan Valley
from other areas of the country and an unusually severe winter,
with blizzards restricting travel to and from the Jordan Valley
on three separate occasions-likely played a role in limiting
the spread of wild poliovirus during the outbreak.
By contrast, wild poliovirus spread was more limited and
resulted in largely subclinical infection in areas of the country
with high seroprevalences of antibodies to polioviruses. In Safi,
a town outside the Jordan Valley where suboptimal immune
response to vaccine was also demonstrated, wild poliovirus
spread appeared to be more extensive. Although the reasons
for largely subclinical infection in most areas outside the Jordan
Valley are unclear, our findings suggest that high population
seroimmunity may have resulted in predominantly silent transmission of wild poliovirus outside the Jordan Valley.
A mass vaccination campaign limited to the Jordan Valley
and nearby areas during the third month of the outbreak did
not prevent wild poliovirus spread to other areas of the country.
By contrast, very few paralytic cases occurred following a
nationwide mass vaccination campaign launched in the fourth
month of the outbreak, despite evidence that wild poliovirus
had already spread beyond the Jordan Valley to other areas of
Jordan. Since the nationwide campaign was launched late in
the outbreak and at a time when cases had already begun to
decline, its true impact is unclear. An alternative explanation
for interruption of wild poliovirus transmission during month
5 of the Jordan outbreak is that high preexisting seroimmunity
to infection among children in most areas outside the Jordan
Valley limited the course of the outbreak. Thus, wild poliovirus
transmission may have ceased as a result of exhaustion of the
pool of susceptibles rather than as a result of the nationwide
mass campaign.
Genotypic studies provide clear evidence that the outbreak
strain was imported [9, 10]. Closer homology of the Jordan
strain with a Pakistan strain than with the Oman outbreak
strain suggests that this represents a separate introduction from
Pakistan rather than spread from a focus in the Middle East.
Although a direct epidemiologic linkage could not be established, the genotypic findings, together with the occurrence of
S70
Reichler et al.
the first case in the outbreak among Pakistani migrant workers,
suggest that importation may have occurred directly into this
community.
In recent years, wild polioviruses imported from the IndiaPakistan subcontinent have been associated with outbreaks in
Oman [3], Malaysia [4], Netherlands [5], and now Jordan. To
prevent recurrent importation, the best long-term solution is to
eradicate wild poliovirus reservoirs in polio-endemic countries
that are major exporters of wild poliovirus, including Pakistan
and India. A nearly 80% reduction in reported poliomyelitis.
cases in Pakistan following national immunization days (NIDs)
in 1994 [19, 20] and India's recent commitment to conduct
NIDs in 1995 and 1996 provide hope that the risk of importation will be reduced in the near future.
The reintroduction and spread of wild poliovirus in the Jordan Valley and subsequently in other areas of Jordan demonstrates the importance of achieving high seroimmunity to infection in all geographic areas to prevent outbreaks caused by
imported strains of wild poliovirus. Until global eradication of
poliomyelitis is accomplished, supplementing routine immunization with mass campaign doses ofOPV-which are believed
to be more immunogenic than OPV delivered through the routine program [21, 22]-and achieving high OPV coverage in
all community subpopulations in a timely fashion may be effective means of ensuring uniformly high population seroimmunity to infection.
Acknowledgments
Weare indebted to Atef Batyneh for encouragement and support; Nadjwa Khouri-Boulos for assistance in evaluating suspected
poliomyelitis cases; Ali Assad, Bassam Hijawi, and physicians
from the Health Directorates in the Jordan Valley for assistance
in conducting fieldwork for the seroepidemiologic studies; Sonia
Russell and Barbara Rice for graphics assistance; and Peter Bing
for helpful comments on the manuscript.
References
1. Paul JR. A history of poliomyelitis. New Haven: Yale University Press,
1971.
2. Strebel PM, Sutter RW, Cochi SL, et al. Epidemiology of poliomyelitis
in the United States one decade after the last reported case of indigenous
wild virus-associated disease. Clin Infect Dis 1992; 14:568-79.
3. SutterRW, Patriarca PA, Brogan S, et al. Outbreak of paralytic poliomyelitis in Oman. Evidence for widespread transmission among fully vaccinated children. Lancet 1991;338:715-20.
4. Centers for Disease Control and Prevention. Progress toward global eradication of poliomyelitis, 1988-1993. MMWR 1994;43:499-503.
TID 1997;175 (Suppll)
5. Oostvogel PM, van Wijngaarden JK, van der Avoort HG, et al. Poliomyelitis outbreak in an unvaccinated community in the Netherlands, 19923. Lancet 1994;344:665-70.
6. Hull HF, Ward NA, Hull BP, Milstien JB, de Quadros C. Paralytic poliomyelitis: seasoned strategies, disappearing disease. Lancet 1994; 343:
1331-7.
7. Melnick JL, Wenner HA, Phillips CA. Enteroviruses. In: Lennette EH,
Schmidt NJ, eds. Diagnostic procedure for viral, rickettsial, and chlamydial infections. Washington DC: American Public Health Association, 1979:471-534.
8. Rico-Hesse R, Pallansch MA, Nottay BK, Kew OM. Geographic distribution of wild poliovirus type 1 genotypes. Virology 1987; 160:311-22.
9. Mulders MN, Lipskaya GY, van der Avoort HGAM, Koopmans MPG,
Kew OM, van Loon AM. Molecular epidemiology of wild poliovirus
type 1 in Europe, the Middle East, and the Indian subcontinent. J Infect
Dis 1995;171:1399-405.
10. Huovilainen A, Mulders M, Agboatwalla M, Poyry T, Stenvik M, Hovi
T. Genetic divergence of poliovirus strains isolated in the Karachi region
of Pakistan. J Gen Virol 1996; 76:3079-88.
11. Orenstein WA, Bernier RH, Dondero TJ, et al. Field evaluation of vaccine
efficacy. Bull WHO 1985;63:1055-68.
12. World Health Organization. Expanded Programme on Immunization. Poliomyelitis outbreak, Bulgaria. Wkly Epidemiol Rec 1992;67:336-7.
13. Strebel P, Aubert-Comiescu A, lon-Nedelcu N, et al. Paralytic poliomyelitis in Romania, 1984-1992: evidence for a high risk of vaccine associated disease and reintroduction of wild-virus infection. Am J Epidemiol
1994; 140:1149-54.
14. Sutter RW, Patriarca PA, Suleiman AJ, et al. Paralytic poliomyelitis in
Oman: association between regional differences in attack rate and variations in antibody responses to oral poliovirus vaccine. lnt J Epidemiol
1993; 22:936-44.
15. John TJ, Jayabal P. Oral poliovirus vaccination in the tropics. The poor
seroconversion rates and the absence of viral interference. Am J Epidemiol 1972;96:263-9.
16. Pangi NS, Master JM, Dave KH. Efficacy of oral polio vaccine in infancy.
Indian Pediatr 1977; 14:523-8.
17. Mahmoud AA, Imam IZ, Abouzid SS, Mished AME, Mitkis FA. The
influence of bacillary dysentery on the efficacy of oral poliovaccine in
Egypt. Gazette Egyptian Paediatr Assoc 1976;24:82-91.
18. Lebaron C, Linkins R, Glass R, et al. Reduction in the immunogenicity of
oral poliovirus vaccine (OPV) following rotavirus infection: preliminary
evidence from Brazil [abstract]. In: Program and abstracts of the 34th
Interscience Conference on Antimicrobial Agents and Chemotherapy
(Orlando). Washington, DC: American Society for Microbiology, 1991:
229.
19. Wahdan MH, Aslanian R, Reichler MR, Gaafar M. Progress toward poliomyelitis eradication in the Eastern Mediterranean Region of the World
Health Organization. J Infect Dis 1997(suppl 1); 175:S50-5.
20. Reichler MR, Aslanian R, Lodhi ZH, et al. Evaluation of oral poliovirus
vaccine delivery during the 1994 national immunization days in Pakistan. J Infect Dis 1997(suppl 1); 175:S205-9.
21. Reichler MR, Kharabsheh S, Rhodes P, et al. Increased immunogenicity
of oral poliovirus vaccine administered in mass vaccination campaigns
compared with the routine vaccination program in Jordan. J Infect Dis
1997(suppl 1); 175:S198-204.
22. Richardson G, Linkins R, Eames M, et al. Immunogenicity of oral poliovirus vaccine administered in mass campaigns versus routine immunization programs. Bull World Health Organ 1995;73:769-77.