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Poliomyelitis in Oman. II. Toward eradication
Acta Tropica 80 (2001) 131– 138 www.parasitology-online.com
Poliomyelitis in Oman. II. Toward eradication Said H.S. Al-Dhahry a,*, Salah T. Al-Awaidy b, Suleman M. Al-Busaidy c, Roshan L. Koul d, Saleh M.S. Al-Khusaiby e, Ali J.M. Suleman f a
Department of Microbiology and Immunology, College of Medicine, Sultan Qaboos Uni6ersity, PO Box 35 Al-Khodh, Muscat 123, Oman b Department of Sur6eillance and Disease Control, Ministry of Health, PO Box 393, Muscat 113, Oman c Central Public Health Laboratory, Ministry of Health, PO Box 393, Muscat 113, Oman d Department of Child Health, Sultan Qaboos Uni6ersity Hospital, PO Box 38, Al-Khodh, Muscat 123, Oman e Department of Child Health, Royal Hospital, Ministry of Health, PO Box 1331, Muscat 111, Oman f Directorate General of Health Affairs, Ministry of Health, PO Box 393, Muscat 113, Oman Received 29 May 2000; received in revised form 10 December 2000; accepted 15 December 2000
Abstract In the past decade, the Sultanate of Oman has experienced three outbreaks of paralytic poliomyelitis— a widespread polio type 1 epidemic in 1988/1989, four cases of polio type 3 in three different regions in 1991, and a localized type 1 outbreak in 1993. The lessons learnt from each of these epidemics have guided us to modify and improve our polio eradication activities. Currently, these activities include administration of five primary and three booster doses of trivalent oral polio vaccine, yearly national immunization campaigns (NIDs) since 1995 with coverage of \90%, localized immunization campaigns, acute flaccid paralysis (AFP) surveillance which involves reporting of all cases by facsimile to the Department of Surveillance within 24 h of detecting a case and weekly zero reporting from 22 sentinel sites, and virological testing of stool specimens of all AFP cases and their close contacts at the national, World Health Organization accredited laboratory. The cumulative success of these activities has resulted in Oman being free from polio for the past 6 years. However, the possibility of importation of wild poliovirus, particularly from southern and western Asia still exists. © 2001 Elsevier Science B.V. All rights reserved. Keywords: Polio eradication; Immunization; Surveillance; Acute flaccid paralysis
1. Introduction In 1988, the World Health Assembly resolved to eradicate poliomyelitis from the world by the year 2000 (World Health Organization, 1988). * Corresponding author. Tel.: + 968-515146; fax: +968513419. E-mail address: [email protected] (S.H.S. Al-Dhahry).
The Eastern Mediterranean Region (EMR) of the World Health Organization (WHO) of which Oman is a member adopted this resolution in the same year. The polio eradication strategies recommended by the WHO were to (1) achieve and maintain high routine immunization coverage with at least three doses of trivalent oral polio vaccine (OPV), (2) implement supplementary immunization activities, including national immu-
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nization days (NIDs) and ‘mopping-up’ operations, (3) develop effective surveillance systems capable of detecting and investigating every case of acute flaccid paralysis (AFP) (Centers for Disease Control and Prevention, 1993). Since the poliomyelitis eradication initiative began, a 95% reduction in the global incidence of polio has been achieved (Aylward et al., 2000). The number of polio-infected countries has decreased from greater than a 100 to 16, in two continents— Asia and Africa, based on data reported to WHO as of August 2000 (Dowdle et al., 1999; World Health Organization, 2000b). However, polio-free zones are emerging in the two continents (Hull et al., 1997; Aylward et al., 2000). In the EMR, the six Arab Gulf states of Oman, Saudi Arabia, United Arab Emirates, Qatar, Bahrain and Kuwait did not report any cases of poliomyelitis in 1998 and 1999, with the exception of a single imported case that was reported from Saudi Arabia in 1998 (World Health Organization, 1999c). Between 1988 and 1993, Oman experienced three outbreaks of paralytic poliomyelitis. A widespread epidemic, which involved 118 cases, lasted from January 1988 to March 1989 (Sutter et al., 1991). Four cases of polio type 3 in three different regions were reported in 1991 (Robertson et al., 1994), and a localized type 1 outbreak occurred in 1993 (unpublished). Lessons learnt from these outbreaks helped us to modify and improve our polio eradication strategy. We report here the development and implementation of Oman’s eradication program that has kept the country free of poliomyelitis for 6 consecutive years.
2. Background Oman has ten health administrative regions and 59 districts (wilayat). Each region has a regional hospital and a regional epidemiologist who reports to the Department of Surveillance and Disease Control (DSDC) at the Ministry of Health headquarters. Health institutions that belong to other government ministries and those of the private sector report directly to the DSDC. As of mid 1998, the population of Oman was 2287640. Fifty five percent of the people resided
in three coastal regions of Muscat, and North and South Batinah (Ministry of Health, 1995). There were 840830 and 272780 children below 15 and 5 years of age, respectively (Directorate General of Planning, 1998). A quarter of the population was expatriates, and the majority (64%) of these came from the Indian sub-continent.
3. Materials and methods
3.1. Routine immunization with oral polio 6accine Prior to the 1988–89 outbreak, a primary series of three doses of OPV was recommended at 3, 5 and 7 months of age, with a booster at 19 months. After the outbreak, the immunization schedule was modified to include five primary doses of OPV —at birth, 40 days, and 3, 5, 7 months of age, and three booster doses— at 19 months, on entering primary school ( 6 years) and on leaving secondary school ( 17 years). Completion of the recommended primary immunization series is required for school entry. Immunization is carried out at all health centers and hospitals of the Ministry of Health, other government hospitals, and 13 approved private clinics. The Ministry of Health provides the vaccine free of charge to all health institutions.
3.2. National immunization days The first NID was conducted in 1995 and was inaugurated by a member of the Royal family. Two rounds of OPV were given a month apart in March and April. Four other NIDs were carried out at yearly intervals, in November and December. In the first three NIDs, OPV was administered to children B 6 years of age, and in the last two, to children B5 years. Vaccination was carried out at the same health units used for routine immunization. However, mobile clinics were used for communities, which could not easily reach the static clinics. Television, radio, newspapers and posters in health units were used to publicize each mass immunization campaign. All NIDs were coordinated with those of other countries within the Gulf co-operation council.
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3.3. Mopping-up immunization campaigns Two intensive, localized (mopping-up) immunization campaigns were carried out in specific districts in Batinah region in 1992 and 1994. Two doses of OPV were administered 1 month apart to children B 5 years of age in a house-to-house operation. These districts were targeted because they were foci of all recent poliomyelitis outbreaks (Sutter et al., 1991; Robertson et al., 1994; unpublished).
3.4. Acute flaccid paralysis sur6eillance An intensive system of surveillance for AFP, with immediate case reporting and rapid investigation to rule out or confirm the diagnosis was established in 1990 (Robertson et al., 1994). Standard case definitions of suspected, probable and confirmed poliomyelitis (de Quadros et al., 1997) were adopted by the Ministry of Health. These definitions and operational guidelines are widely publicized (Ministry of Health, 1995). Modifications to the guidelines include simultaneous reporting by telephone or facsimile of each AFP case to the district, regional and national levels and to the University Hospital. All AFP cases are referred to the pediatric neurologist at the University Hospital; only in exceptional circumstances are patients treated in other hospitals but in consultation with the pediatric neurologist.
3.5. Laboratory sur6eillance Stool samples are obtained from AFP cases and a minimum of five contacts aged B6 years for each case. Although the WHO’s recommendations call for the collection of at least two stool specimens 24– 48 h apart and within 14 days of onset of symptoms (Hull and Dowdle, 1997), the recommendation of the national polio expert committee is a minimum of three samples. Each stool sample from an AFP case is processed in two laboratories—at the University Hospital and the Central Public Health laboratory using established procedures for isolation and typing of virus isolates (World Health Organization, 1992). Experience from the Americas showed that testing
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stool specimens obtained from persons with AFP in whom there is strong clinical suspicion of poliomyelitis in two or more laboratories increases the probability of detecting wild poliovirus (de Quadros et al., 1997). However, this is not a universal practice, nor is it a WHO recommendation. The Central Public Health laboratory is a national laboratory that has been accredited by WHO since 1997, and is a part of the global laboratory network (World Health Organization, 2000a). It processes all stool specimens from contacts of AFP patients. Until recently, poliovirus isolates were sent to the Centers for Disease Control and Prevention, Atlanta, GA, for confirmation and intratypic differentiation. Currently, they are sent to the regional reference laboratory in Kuwait.
3.6. Reporting and feedback Standard forms are used for case notification and case investigation by clinicians and epidemiologists, respectively. The 22 sentinel sites across the country report weekly by facsimile on the presence or absence of AFP cases (i.e. negative or zero reporting) to the national level, where a check list for receipt and completeness of these reports is updated weekly. Until mid 1999, AFP and laboratory surveillance data were sent weekly by facsimile to EMR headquarters. They are currently sent by electronic mail. Feedback to personnel involved in the national polio eradication program is through several channels. The physician who refers the patient gets a medical report. A quarterly communicable disease surveillance newsletter is distributed to all health units and the communicable disease statistical report, which is updated regularly, is sent to superintendents of regional hospitals by e-mail.
4. Results
4.1. Co6erage with oral polio 6accine and occurrence of poliomyelitis The Expanded Programme on Immunization (EPI) in Oman began in 1981. Coverage with at
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least three doses of OPV increased from 23% in 1982 to 83% in 1987 (Fig. 1), just before the country experienced a widespread poliovirus type 1 outbreak (Sutter et al., 1991). Coverage reached 96% in 1989, and remained at this high level until 1999. During the period from 1990 to 1993, there were six cases of poliomyelitis. There were no polio cases from 1994 to 1999 and none has been detected during the first 10 months of 2000.
4.2. Supplementary immunization Each of the two rounds of the first NID in 1995 was completed in 6 days. Subsequent campaigns were conducted in 2 or 3 days. The national average coverage varied from 87 to 99% (Fig. 2). The lowest coverage was 70% in one region in 1995 (data not shown). This improved to 80% in 1996, 87% in 1997, and 92% in 1998 and 1999. High OPV coverage (\ 90%) was also achieved in the two mopping-up campaigns.
4.3. Acute flaccid paralysis sur6eillance From 1996 to 1999, weekly reports were received from all sentinel sites. The number of AFP cases reported by these sites, as well as laboratory and demographic data were used to calculate the annual rate of AFP not due to polio per 100000 population aged B 15 years (Table 1). Results of other AFP performance indicators that were monitored during the same period are also shown in Table 1. Although the minimum targets were met for all indicators, there was some delay in notification of cases to the national health authorities. The rate of non-polio AFP cases was 1.3 per 100000 children B 15 years of age in 1990. From 1991 to 1995, the annual rates were 2.3, 2.3, 2.2, 2.5 and 2.7, respectively. Thus, for 10 consecutive years, the annual rate has been E1. Forty percent of the non-polio AFP cases were Guillian-Barre syndrome. Other less common diagnoses included transient mononeuritis, acute viral radiculomyositis, and upper motor neurone monoparesis.
Fig. 1. Coverage with three doses of trivalent oral polio vaccine by 1 year of age and reported cases of paralytic poliomyelitis in Oman, 1981 – 1999.
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Fig. 2. Coverage with trivalent oral polio vaccine in each round of the National Immunization days conducted in Oman from 1995 to 1999.
During the period 1996– 1999, two regions (Sharkiya and Dhahira), with respectively 107000 and 78000 children B15 years of age, did not report any case of AFP for 3 consecutive years. This probably contributed to the drop in the AFP rate recorded in 1996– 1998. AFP cases were also not reported for E3 years from the sparsely populated regions of Musandam and Al Wousta (population below 15 years 12580 and 7000, respectively).
4.4. Laboratory sur6eillance Between 1996 and 1999, a total of 186 stool specimens were collected from 54 children suspected of poliomyelitis (average 3.4 stool specimens per patient) (Table 2). All were received within 3 days in good condition and results were sent to the attending pediatrician and the DSDC within 4 weeks of receipt of the sample. Within
the same period, 681 stool samples from contacts of AFP cases were examined (average, 12.6 contact stool specimens per patient). The isolation rate of non-polio enteroviruses (NPEV) from healthy children varied from 18.2 to 30%. The overall NPEV isolation rates for patients and contacts were 16.6, 25.6, 26.7, and 17.4% for 1996– 1999, respectively. Echo, Coxsackie A and Coxsackie B viruses constituted, respectively, 31, 2.2 and 13.8% of the isolates. Other NPEV could not be typed due to unavailability of typing sera. Polio Sabin vaccine virus was isolated from five healthy children. Four isolates were type 1 and one was type 3.
5. Discussion The polio eradication strategies recommended by the WHO formed the basis for development of
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national eradication programs. The foundation on which the eradication initiative was built was a high immunization coverage with OPV delivered through primary health care systems (Expanded Programme on Immunization, 1993). When the EPI began in Oman in 1981, the recommended vaccination schedule for polio was a primary series of three doses of OPV at 3, 5, and 7 months and a booster dose at 19 months. Although coverage of children by their first birthday with the primary series of OPV had reached 83% by the end of 1987, a widespread polio type 1 outbreak occurred in 1988– 1989 (Sutter et al., 1991). The change in the immunization schedule to five primary doses, and immunization coverage E 95% since 1990 has been associated with a dramatic decline in the incidence of poliomyelitis in Oman. The WHO recommends that infants receive four doses of OPV at birth, and at 6, 10, and 14 weeks of age, and that countries should aim to vaccinate at least 90% of infants against polio by 1 year of age (Hull et al., 1997). Despite meeting these goals, smaller polio outbreaks continued to occur in Oman (Robertson et al., 1994; unpublished). Our experience that routine immunization that leaves pockets of unprotected children could not eradicate polio had been observed in other countries (Hull et al., 1994). Thus, supplementary immunization activities of NIDs, immunization in response to outbreaks, and mopping-up operations were all implemented. The NIDs conducted in this country for the past 5 years had high overall coverage. During the same period, there were no cases of paralytic poliomyelitis and wild
poliovirus was not detected. Mass campaigns interrupt wild poliovirus transmission by rapidly increasing systemic and intestinal immunity in the population (Birmingham et al., 1997b). The scientific basis for the success of mass campaigns was provided by Reichler et al. who demonstrated that OPV delivered in campaigns is more immunogenic dose-for-dose than OPV delivered through routine immunization, possibly as a result of multiple exposures to vaccine virus over a short time period (Reichler et al., 1997). Co-ordination of NIDs among Arab Gulf states has contributed to the emergence of a polio-free zone within the East Mediterranean region (Wahdan et al., 1997). An active surveillance system that monitors the incidence of AFP and ascertains that cases are not due to wild polioviruses is a critical component of the polio eradication strategy. An effective system should detect at least one case of AFP per year per 100000 population B 15 years of age (de Quadros et al., 1997). In Oman, an enhanced AFP surveillance system replaced a passive system after the 1988– 1989 polio outbreak, and has been operational since 1990 (Hull et al., 1994; Robertson et al., 1994). The surveillance system, which has consistently met the minimum AFP detection criteria, led to early detection, and timely response to polio outbreaks in 1991 (Robertson et al., 1994) and 1993 (unpublished). The ultimate goal of polio eradication is to stop forever the transmission of wild polioviruses among the human population and to eliminate any chance that the virus can start circulating again. When that goal is achieved, there will be no
Table 1 Performance indicators for AFP surveillance, Oman 1996–1999 Indicator
Target
Year 1996
Non-polio AFP rate in children B15 years old AFP cases detected within 7 days of paralysis AFP cases notified to public health authorities within 24 h Reported AFP cases investigated within 48 h Reported AFP cases with two stool specimens collected 24–48 h apart within 14 days of paralysis One stool sample collected from each of five contacts
1997
1998
1999
E1/100 000 E80% E80% E80% E80%
1.2 1.0 80% 100% 90% 75% 100% 100% 100% 100%
1.0 86% 100% 100% 89%
2.7 83% 83% 100% 91%
E80%
100% 100%
100%
100%
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Table 2 Laboratory surveillance of AFP cases and contacts Year
Number of AFP cases investigated
Total number of patient stools tested
Number (%) of patient Total number of stool positive for contact stools tested NPEVa
Number (%) contact stools positive for NPEV
1996 1997 1998 1999
10 8 13 23
43 22 44 77
2 1 16 11
26 33 44 50
a
(4.7) (4.5) (36.3) (15.5)
126 110 171 274
(20.6) (30.0) (25.7) (18.2)
Non polio enteroviruses.
cases of clinical poliomyelitis caused by wild polioviruses, and no wild polioviruses will be found despite intensive efforts to do so (Birmingham et al., 1997a; Hull et al., 1997). Thus, poliovirus surveillance will provide the evidence for certification of eradication. Laboratory testing for enteroviruses, including polioviruses, of healthy children who come into contact with AFP patients provides the ideal opportunity to detect the presence of wild polioviruses in a community. A national laboratory is required to test a minimum of 150 stool specimens per year, and isolate enteroviruses from E10% of all specimens tested (Hull and Dowdle, 1997). The collection of stool specimens from an average of 12 contacts per AFP case enabled us to achieve the recommended target for effective virological surveillance. The isolation rate of non-polio enteroviruses in Oman is high when compared to the average rate of 9% for the EMR (World Health Organization, 1999b). Comparable rates have been reported from Kenya (Expanded Programme on Immunization, 1992), the Peoples Republic of China (Jian et al., 1997) and Nepal (World Health Organization, 1999a). Since NPEV isolation rate is greatly influenced by latitude, altitude, hygiene and climate, it would be more appropriate to compare our data with those from countries within the Arabian Gulf and the Middle East. However, there is no published data from these countries. Two regions in Oman with sizeable populations of children B 15 years of age did not report any AFP cases for at least 3 consecutive years. The importance of maintaining high quality epidemiological and laboratory surveillance at subnational
level was recently highlighted by undetected circulation for periods of 24 months of wild poliovirus type 3 in Egypt and wild virus type 1 in Iraq (World Health Organization, 1999b). In recognition of this, a national seminar to reinforce the polio eradication initiative was conducted in Oman in June 1999. Regions whose AFP surveillance system needed improvement were particularly targeted. Oman has sustained a very high (\ 95%) coverage with OPV among infants for the past 10 years. The supplementary immunization activities have covered at least 90% of the target population. There is in place an effective epidemiological and virological surveillance system. Our observations that (a) polio outbreaks of 1991 and 1993 were geographically restricted to a few regions and involved very small numbers of children, (b) no polio cases have occurred during the past 6 years, and (c) wild poliovirus has not been isolated from any AFP case nor from their contacts during the same period provide evidence that the program has been successful. This success has been a result of many factors, including strong national commitment to the program, well-developed health, communication and information infrastructure, teamwork among surveillance partners (EPI nurses and managers, clinicians, epidemiologists, and virologists), and the public’s co-operation. The relative small population in relation to availability of financial and other resources was also a significant factor. The greatest challenge is to maintain this polio-free status until wild poliovirus ceases to circulate in countries where polio is still endemic.
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References Aylward, R.B., Hull, H.F., Cochi, S.L., Sutter, R.W., Olive, J.-M., Melgaard, B., 2000. Disease eradication as a public health strategy: a case study of poliomyelitis eradication. Bull. World Health Organ. 78, 285 –297. Birmingham, M.E., Linkins, R.W., Hull, B.P., Hull, H.F., 1997a. Poliomyelitis surveillance: the compass for eradication. J. Infect. Dis. 175 (Suppl. 1), S146 –S150. Birmingham, M.E., Aylward, R.B., Cochi, S.L., Hull, H.F., 1997b. National immunization days: state of the art. J. Infect. Dis. 175 (Suppl. 1), S183 – S188. Centers for Disease Control and Prevention, 1993. Progress toward global eradication of poliomyelitis, 1988 – 1991. MMWR Morb. Mort. Wkly Rep. 42, pp. 486–495. de Quadros, C.A., Hersch, B.S., Olive, J.M., Andrus, J.K., da Silveira, C.M., Carraso, P.A., 1997. Eradication of wild poliovirus from the Americas: acute flaccid paralysis surveillance, 1988 – 1995. J. Infect. Dis. 175 (Suppl. 1), S37– S42. Directorate General of Planning, 1998. Sultanate of Oman Health Facts. Ministry of Health, Sultanate of Oman. Dowdle, W.R., Featherstone, D.A., Birmingham, M.E., Hull, H.F., Aylward, R.B., 1999. Poliomyelitis eradication. Virus Res. 62, 185 – 192. Expanded Programme on Immunization, 1992. Serological and virological assessment of oral and inactivated poliovirus vaccines in a rural population. Wkly. Epidemiol. Rec. 67, pp. 179 – 182. Expanded Programme on Immunization, 1993. Poliomyelitis in 1992. Wkly. Epidemiol. Rec. 68, pp. 225 –230. Hull, H.F., Ward, N.A., Hull, B.P., Milstein, J.B., de Quadros, C., 1994. Paralytic poliomyelitis: seasoned strategies, disappearing disease. Lancet 343, 1331 –1337. Hull, B.P., Dowdle, W.R., 1997. Poliovirus surveillance: building the global polio laboratory network. J. Infect. Dis. 175 (Suppl. 1), S113 – S116. Hull, H.F., Birmingham, M.E., Melgard, B., Lee, J.W., 1997. Progress toward global polio eradication. J. Infect. Dis. 175 (Suppl. 1), S4 – S9. Jian, Z., Li-bi, Z., Otten, M.W., Tao, J., Xing-lu, Z., Rongzhen, Z., Ke-an, W., 1997. Surveillance for polio eradication in the Peoples Republic of China. J. Infect. Dis. 175 (Suppl. 1), S122 – S134. Ministry of Health, 1995. Progress toward poliomyelitis eradication –Oman: acute flaccid paralysis surveillance, 1990 –
1995. Community Health and Disease Surveillance Newsletter IV, pp. 1 – 5. Reichler, M.R., Kharabsheh, S., Rhodes, P., Otoum, H., Bloch, S., Majid, A.M., Pallansch, M.A., Patriarca, P.A., Cochi, S.L., 1997. Increased immunogenicity of oral poliovirus vaccine administered in mass vaccination campaigns compared with routine vaccination program in Jordan. J. Infect. Dis. 175 (Suppl 1), S198 – S204. Robertson, S.E., Suleiman, A.J.M., Mehta, F.R., Al-Dhahry, S.H.S., El-Bualy, M.S., 1994. Poliomyelitis in Oman: acute flaccid paralysis surveillance leading to early detection and rapid response to a type 3 outbreak. Bull. World Health Organ. 72, 907 – 914. Sutter, R.W., Patriarca, P.A., Brogan, S., Malankar, P.G., Pallansch, M.A., Kew, O.M., Bass, A.G., Cochi, S.L., Alexander, J.P., Hall, D.B., Suleiman, A.J.M., Al-Ghassany, A.A.K., El-Bualy, M.S., 1991. Outbreak of paralytic poliomyelitis in Oman: evidence for widespread transmission among fully vaccinated children. Lancet 338, 715 – 720. Wahdan, M.H., Aslanian, R., Reichler, M.R., Gafaar, M.T., 1997. Progress toward poliomyelitis eradication in the Eastern Mediterranean Region of the World Health Organization. J. Infect. Dis. 175 (Suppl. 1), S50 – S55. World Health Organization, 1988. Global eradication of poliomyelitis by the year 2000. Wkly. Epidemiol. Rec. 63, pp. 161 – 168. World Health Organization, 1992. Manual for the Virological Investigation of Poliomyelitis. Geneva. WHO/EPI/CDS/ POLIO 90.1. World Health Organization, 1999a. Progress towards poliomyelitis eradication, Nepal 1996 – 1999. Wkly. Epidemiol. Rec. 74, pp. 349 – 353. World Health Organization, 1999b. Progress towards poliomyelitis eradication, WHO Eastern Mediterranean Region. Wkly. Epidemiol. Rec. 74, pp. 405 – 408. World Health Organization. (1999c) Performance of acute flaccid paralysis surveillance and incidence of poliomyelitis, 1998 – 1999. Wkly. Epidemiol. Rec. 74, pp. 421 – 424. World Health Organization, 2000a. Global laboratory network for poliomyelitis eradication, 1997 – 1999: development and expanding contributions. Wkly. Epidemiol. Rec. 75, pp. 70 – 75. World Health Organization, 2000b. Performance of acute flaccid paralysis (AFP) surveillance and incidence of poliomyelitis, 1999 – 2000. Wkly. Epidemiol. Rec. 75, pp. 298 – 301.
Poliomyelitis in Oman. II. Toward eradication Said H.S. Al-Dhahry a,*, Salah T. Al-Awaidy b, Suleman M. Al-Busaidy c, Roshan L. Koul d, Saleh M.S. Al-Khusaiby e, Ali J.M. Suleman f a
Department of Microbiology and Immunology, College of Medicine, Sultan Qaboos Uni6ersity, PO Box 35 Al-Khodh, Muscat 123, Oman b Department of Sur6eillance and Disease Control, Ministry of Health, PO Box 393, Muscat 113, Oman c Central Public Health Laboratory, Ministry of Health, PO Box 393, Muscat 113, Oman d Department of Child Health, Sultan Qaboos Uni6ersity Hospital, PO Box 38, Al-Khodh, Muscat 123, Oman e Department of Child Health, Royal Hospital, Ministry of Health, PO Box 1331, Muscat 111, Oman f Directorate General of Health Affairs, Ministry of Health, PO Box 393, Muscat 113, Oman Received 29 May 2000; received in revised form 10 December 2000; accepted 15 December 2000
Abstract In the past decade, the Sultanate of Oman has experienced three outbreaks of paralytic poliomyelitis— a widespread polio type 1 epidemic in 1988/1989, four cases of polio type 3 in three different regions in 1991, and a localized type 1 outbreak in 1993. The lessons learnt from each of these epidemics have guided us to modify and improve our polio eradication activities. Currently, these activities include administration of five primary and three booster doses of trivalent oral polio vaccine, yearly national immunization campaigns (NIDs) since 1995 with coverage of \90%, localized immunization campaigns, acute flaccid paralysis (AFP) surveillance which involves reporting of all cases by facsimile to the Department of Surveillance within 24 h of detecting a case and weekly zero reporting from 22 sentinel sites, and virological testing of stool specimens of all AFP cases and their close contacts at the national, World Health Organization accredited laboratory. The cumulative success of these activities has resulted in Oman being free from polio for the past 6 years. However, the possibility of importation of wild poliovirus, particularly from southern and western Asia still exists. © 2001 Elsevier Science B.V. All rights reserved. Keywords: Polio eradication; Immunization; Surveillance; Acute flaccid paralysis
1. Introduction In 1988, the World Health Assembly resolved to eradicate poliomyelitis from the world by the year 2000 (World Health Organization, 1988). * Corresponding author. Tel.: + 968-515146; fax: +968513419. E-mail address: [email protected] (S.H.S. Al-Dhahry).
The Eastern Mediterranean Region (EMR) of the World Health Organization (WHO) of which Oman is a member adopted this resolution in the same year. The polio eradication strategies recommended by the WHO were to (1) achieve and maintain high routine immunization coverage with at least three doses of trivalent oral polio vaccine (OPV), (2) implement supplementary immunization activities, including national immu-
0001-706X/01/$ - see front matter © 2001 Elsevier Science B.V. All rights reserved. PII: S0001-706X(01)00167-X
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nization days (NIDs) and ‘mopping-up’ operations, (3) develop effective surveillance systems capable of detecting and investigating every case of acute flaccid paralysis (AFP) (Centers for Disease Control and Prevention, 1993). Since the poliomyelitis eradication initiative began, a 95% reduction in the global incidence of polio has been achieved (Aylward et al., 2000). The number of polio-infected countries has decreased from greater than a 100 to 16, in two continents— Asia and Africa, based on data reported to WHO as of August 2000 (Dowdle et al., 1999; World Health Organization, 2000b). However, polio-free zones are emerging in the two continents (Hull et al., 1997; Aylward et al., 2000). In the EMR, the six Arab Gulf states of Oman, Saudi Arabia, United Arab Emirates, Qatar, Bahrain and Kuwait did not report any cases of poliomyelitis in 1998 and 1999, with the exception of a single imported case that was reported from Saudi Arabia in 1998 (World Health Organization, 1999c). Between 1988 and 1993, Oman experienced three outbreaks of paralytic poliomyelitis. A widespread epidemic, which involved 118 cases, lasted from January 1988 to March 1989 (Sutter et al., 1991). Four cases of polio type 3 in three different regions were reported in 1991 (Robertson et al., 1994), and a localized type 1 outbreak occurred in 1993 (unpublished). Lessons learnt from these outbreaks helped us to modify and improve our polio eradication strategy. We report here the development and implementation of Oman’s eradication program that has kept the country free of poliomyelitis for 6 consecutive years.
2. Background Oman has ten health administrative regions and 59 districts (wilayat). Each region has a regional hospital and a regional epidemiologist who reports to the Department of Surveillance and Disease Control (DSDC) at the Ministry of Health headquarters. Health institutions that belong to other government ministries and those of the private sector report directly to the DSDC. As of mid 1998, the population of Oman was 2287640. Fifty five percent of the people resided
in three coastal regions of Muscat, and North and South Batinah (Ministry of Health, 1995). There were 840830 and 272780 children below 15 and 5 years of age, respectively (Directorate General of Planning, 1998). A quarter of the population was expatriates, and the majority (64%) of these came from the Indian sub-continent.
3. Materials and methods
3.1. Routine immunization with oral polio 6accine Prior to the 1988–89 outbreak, a primary series of three doses of OPV was recommended at 3, 5 and 7 months of age, with a booster at 19 months. After the outbreak, the immunization schedule was modified to include five primary doses of OPV —at birth, 40 days, and 3, 5, 7 months of age, and three booster doses— at 19 months, on entering primary school ( 6 years) and on leaving secondary school ( 17 years). Completion of the recommended primary immunization series is required for school entry. Immunization is carried out at all health centers and hospitals of the Ministry of Health, other government hospitals, and 13 approved private clinics. The Ministry of Health provides the vaccine free of charge to all health institutions.
3.2. National immunization days The first NID was conducted in 1995 and was inaugurated by a member of the Royal family. Two rounds of OPV were given a month apart in March and April. Four other NIDs were carried out at yearly intervals, in November and December. In the first three NIDs, OPV was administered to children B 6 years of age, and in the last two, to children B5 years. Vaccination was carried out at the same health units used for routine immunization. However, mobile clinics were used for communities, which could not easily reach the static clinics. Television, radio, newspapers and posters in health units were used to publicize each mass immunization campaign. All NIDs were coordinated with those of other countries within the Gulf co-operation council.
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3.3. Mopping-up immunization campaigns Two intensive, localized (mopping-up) immunization campaigns were carried out in specific districts in Batinah region in 1992 and 1994. Two doses of OPV were administered 1 month apart to children B 5 years of age in a house-to-house operation. These districts were targeted because they were foci of all recent poliomyelitis outbreaks (Sutter et al., 1991; Robertson et al., 1994; unpublished).
3.4. Acute flaccid paralysis sur6eillance An intensive system of surveillance for AFP, with immediate case reporting and rapid investigation to rule out or confirm the diagnosis was established in 1990 (Robertson et al., 1994). Standard case definitions of suspected, probable and confirmed poliomyelitis (de Quadros et al., 1997) were adopted by the Ministry of Health. These definitions and operational guidelines are widely publicized (Ministry of Health, 1995). Modifications to the guidelines include simultaneous reporting by telephone or facsimile of each AFP case to the district, regional and national levels and to the University Hospital. All AFP cases are referred to the pediatric neurologist at the University Hospital; only in exceptional circumstances are patients treated in other hospitals but in consultation with the pediatric neurologist.
3.5. Laboratory sur6eillance Stool samples are obtained from AFP cases and a minimum of five contacts aged B6 years for each case. Although the WHO’s recommendations call for the collection of at least two stool specimens 24– 48 h apart and within 14 days of onset of symptoms (Hull and Dowdle, 1997), the recommendation of the national polio expert committee is a minimum of three samples. Each stool sample from an AFP case is processed in two laboratories—at the University Hospital and the Central Public Health laboratory using established procedures for isolation and typing of virus isolates (World Health Organization, 1992). Experience from the Americas showed that testing
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stool specimens obtained from persons with AFP in whom there is strong clinical suspicion of poliomyelitis in two or more laboratories increases the probability of detecting wild poliovirus (de Quadros et al., 1997). However, this is not a universal practice, nor is it a WHO recommendation. The Central Public Health laboratory is a national laboratory that has been accredited by WHO since 1997, and is a part of the global laboratory network (World Health Organization, 2000a). It processes all stool specimens from contacts of AFP patients. Until recently, poliovirus isolates were sent to the Centers for Disease Control and Prevention, Atlanta, GA, for confirmation and intratypic differentiation. Currently, they are sent to the regional reference laboratory in Kuwait.
3.6. Reporting and feedback Standard forms are used for case notification and case investigation by clinicians and epidemiologists, respectively. The 22 sentinel sites across the country report weekly by facsimile on the presence or absence of AFP cases (i.e. negative or zero reporting) to the national level, where a check list for receipt and completeness of these reports is updated weekly. Until mid 1999, AFP and laboratory surveillance data were sent weekly by facsimile to EMR headquarters. They are currently sent by electronic mail. Feedback to personnel involved in the national polio eradication program is through several channels. The physician who refers the patient gets a medical report. A quarterly communicable disease surveillance newsletter is distributed to all health units and the communicable disease statistical report, which is updated regularly, is sent to superintendents of regional hospitals by e-mail.
4. Results
4.1. Co6erage with oral polio 6accine and occurrence of poliomyelitis The Expanded Programme on Immunization (EPI) in Oman began in 1981. Coverage with at
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least three doses of OPV increased from 23% in 1982 to 83% in 1987 (Fig. 1), just before the country experienced a widespread poliovirus type 1 outbreak (Sutter et al., 1991). Coverage reached 96% in 1989, and remained at this high level until 1999. During the period from 1990 to 1993, there were six cases of poliomyelitis. There were no polio cases from 1994 to 1999 and none has been detected during the first 10 months of 2000.
4.2. Supplementary immunization Each of the two rounds of the first NID in 1995 was completed in 6 days. Subsequent campaigns were conducted in 2 or 3 days. The national average coverage varied from 87 to 99% (Fig. 2). The lowest coverage was 70% in one region in 1995 (data not shown). This improved to 80% in 1996, 87% in 1997, and 92% in 1998 and 1999. High OPV coverage (\ 90%) was also achieved in the two mopping-up campaigns.
4.3. Acute flaccid paralysis sur6eillance From 1996 to 1999, weekly reports were received from all sentinel sites. The number of AFP cases reported by these sites, as well as laboratory and demographic data were used to calculate the annual rate of AFP not due to polio per 100000 population aged B 15 years (Table 1). Results of other AFP performance indicators that were monitored during the same period are also shown in Table 1. Although the minimum targets were met for all indicators, there was some delay in notification of cases to the national health authorities. The rate of non-polio AFP cases was 1.3 per 100000 children B 15 years of age in 1990. From 1991 to 1995, the annual rates were 2.3, 2.3, 2.2, 2.5 and 2.7, respectively. Thus, for 10 consecutive years, the annual rate has been E1. Forty percent of the non-polio AFP cases were Guillian-Barre syndrome. Other less common diagnoses included transient mononeuritis, acute viral radiculomyositis, and upper motor neurone monoparesis.
Fig. 1. Coverage with three doses of trivalent oral polio vaccine by 1 year of age and reported cases of paralytic poliomyelitis in Oman, 1981 – 1999.
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Fig. 2. Coverage with trivalent oral polio vaccine in each round of the National Immunization days conducted in Oman from 1995 to 1999.
During the period 1996– 1999, two regions (Sharkiya and Dhahira), with respectively 107000 and 78000 children B15 years of age, did not report any case of AFP for 3 consecutive years. This probably contributed to the drop in the AFP rate recorded in 1996– 1998. AFP cases were also not reported for E3 years from the sparsely populated regions of Musandam and Al Wousta (population below 15 years 12580 and 7000, respectively).
4.4. Laboratory sur6eillance Between 1996 and 1999, a total of 186 stool specimens were collected from 54 children suspected of poliomyelitis (average 3.4 stool specimens per patient) (Table 2). All were received within 3 days in good condition and results were sent to the attending pediatrician and the DSDC within 4 weeks of receipt of the sample. Within
the same period, 681 stool samples from contacts of AFP cases were examined (average, 12.6 contact stool specimens per patient). The isolation rate of non-polio enteroviruses (NPEV) from healthy children varied from 18.2 to 30%. The overall NPEV isolation rates for patients and contacts were 16.6, 25.6, 26.7, and 17.4% for 1996– 1999, respectively. Echo, Coxsackie A and Coxsackie B viruses constituted, respectively, 31, 2.2 and 13.8% of the isolates. Other NPEV could not be typed due to unavailability of typing sera. Polio Sabin vaccine virus was isolated from five healthy children. Four isolates were type 1 and one was type 3.
5. Discussion The polio eradication strategies recommended by the WHO formed the basis for development of
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national eradication programs. The foundation on which the eradication initiative was built was a high immunization coverage with OPV delivered through primary health care systems (Expanded Programme on Immunization, 1993). When the EPI began in Oman in 1981, the recommended vaccination schedule for polio was a primary series of three doses of OPV at 3, 5, and 7 months and a booster dose at 19 months. Although coverage of children by their first birthday with the primary series of OPV had reached 83% by the end of 1987, a widespread polio type 1 outbreak occurred in 1988– 1989 (Sutter et al., 1991). The change in the immunization schedule to five primary doses, and immunization coverage E 95% since 1990 has been associated with a dramatic decline in the incidence of poliomyelitis in Oman. The WHO recommends that infants receive four doses of OPV at birth, and at 6, 10, and 14 weeks of age, and that countries should aim to vaccinate at least 90% of infants against polio by 1 year of age (Hull et al., 1997). Despite meeting these goals, smaller polio outbreaks continued to occur in Oman (Robertson et al., 1994; unpublished). Our experience that routine immunization that leaves pockets of unprotected children could not eradicate polio had been observed in other countries (Hull et al., 1994). Thus, supplementary immunization activities of NIDs, immunization in response to outbreaks, and mopping-up operations were all implemented. The NIDs conducted in this country for the past 5 years had high overall coverage. During the same period, there were no cases of paralytic poliomyelitis and wild
poliovirus was not detected. Mass campaigns interrupt wild poliovirus transmission by rapidly increasing systemic and intestinal immunity in the population (Birmingham et al., 1997b). The scientific basis for the success of mass campaigns was provided by Reichler et al. who demonstrated that OPV delivered in campaigns is more immunogenic dose-for-dose than OPV delivered through routine immunization, possibly as a result of multiple exposures to vaccine virus over a short time period (Reichler et al., 1997). Co-ordination of NIDs among Arab Gulf states has contributed to the emergence of a polio-free zone within the East Mediterranean region (Wahdan et al., 1997). An active surveillance system that monitors the incidence of AFP and ascertains that cases are not due to wild polioviruses is a critical component of the polio eradication strategy. An effective system should detect at least one case of AFP per year per 100000 population B 15 years of age (de Quadros et al., 1997). In Oman, an enhanced AFP surveillance system replaced a passive system after the 1988– 1989 polio outbreak, and has been operational since 1990 (Hull et al., 1994; Robertson et al., 1994). The surveillance system, which has consistently met the minimum AFP detection criteria, led to early detection, and timely response to polio outbreaks in 1991 (Robertson et al., 1994) and 1993 (unpublished). The ultimate goal of polio eradication is to stop forever the transmission of wild polioviruses among the human population and to eliminate any chance that the virus can start circulating again. When that goal is achieved, there will be no
Table 1 Performance indicators for AFP surveillance, Oman 1996–1999 Indicator
Target
Year 1996
Non-polio AFP rate in children B15 years old AFP cases detected within 7 days of paralysis AFP cases notified to public health authorities within 24 h Reported AFP cases investigated within 48 h Reported AFP cases with two stool specimens collected 24–48 h apart within 14 days of paralysis One stool sample collected from each of five contacts
1997
1998
1999
E1/100 000 E80% E80% E80% E80%
1.2 1.0 80% 100% 90% 75% 100% 100% 100% 100%
1.0 86% 100% 100% 89%
2.7 83% 83% 100% 91%
E80%
100% 100%
100%
100%
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Table 2 Laboratory surveillance of AFP cases and contacts Year
Number of AFP cases investigated
Total number of patient stools tested
Number (%) of patient Total number of stool positive for contact stools tested NPEVa
Number (%) contact stools positive for NPEV
1996 1997 1998 1999
10 8 13 23
43 22 44 77
2 1 16 11
26 33 44 50
a
(4.7) (4.5) (36.3) (15.5)
126 110 171 274
(20.6) (30.0) (25.7) (18.2)
Non polio enteroviruses.
cases of clinical poliomyelitis caused by wild polioviruses, and no wild polioviruses will be found despite intensive efforts to do so (Birmingham et al., 1997a; Hull et al., 1997). Thus, poliovirus surveillance will provide the evidence for certification of eradication. Laboratory testing for enteroviruses, including polioviruses, of healthy children who come into contact with AFP patients provides the ideal opportunity to detect the presence of wild polioviruses in a community. A national laboratory is required to test a minimum of 150 stool specimens per year, and isolate enteroviruses from E10% of all specimens tested (Hull and Dowdle, 1997). The collection of stool specimens from an average of 12 contacts per AFP case enabled us to achieve the recommended target for effective virological surveillance. The isolation rate of non-polio enteroviruses in Oman is high when compared to the average rate of 9% for the EMR (World Health Organization, 1999b). Comparable rates have been reported from Kenya (Expanded Programme on Immunization, 1992), the Peoples Republic of China (Jian et al., 1997) and Nepal (World Health Organization, 1999a). Since NPEV isolation rate is greatly influenced by latitude, altitude, hygiene and climate, it would be more appropriate to compare our data with those from countries within the Arabian Gulf and the Middle East. However, there is no published data from these countries. Two regions in Oman with sizeable populations of children B 15 years of age did not report any AFP cases for at least 3 consecutive years. The importance of maintaining high quality epidemiological and laboratory surveillance at subnational
level was recently highlighted by undetected circulation for periods of 24 months of wild poliovirus type 3 in Egypt and wild virus type 1 in Iraq (World Health Organization, 1999b). In recognition of this, a national seminar to reinforce the polio eradication initiative was conducted in Oman in June 1999. Regions whose AFP surveillance system needed improvement were particularly targeted. Oman has sustained a very high (\ 95%) coverage with OPV among infants for the past 10 years. The supplementary immunization activities have covered at least 90% of the target population. There is in place an effective epidemiological and virological surveillance system. Our observations that (a) polio outbreaks of 1991 and 1993 were geographically restricted to a few regions and involved very small numbers of children, (b) no polio cases have occurred during the past 6 years, and (c) wild poliovirus has not been isolated from any AFP case nor from their contacts during the same period provide evidence that the program has been successful. This success has been a result of many factors, including strong national commitment to the program, well-developed health, communication and information infrastructure, teamwork among surveillance partners (EPI nurses and managers, clinicians, epidemiologists, and virologists), and the public’s co-operation. The relative small population in relation to availability of financial and other resources was also a significant factor. The greatest challenge is to maintain this polio-free status until wild poliovirus ceases to circulate in countries where polio is still endemic.
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References Aylward, R.B., Hull, H.F., Cochi, S.L., Sutter, R.W., Olive, J.-M., Melgaard, B., 2000. Disease eradication as a public health strategy: a case study of poliomyelitis eradication. Bull. World Health Organ. 78, 285 –297. Birmingham, M.E., Linkins, R.W., Hull, B.P., Hull, H.F., 1997a. Poliomyelitis surveillance: the compass for eradication. J. Infect. Dis. 175 (Suppl. 1), S146 –S150. Birmingham, M.E., Aylward, R.B., Cochi, S.L., Hull, H.F., 1997b. National immunization days: state of the art. J. Infect. Dis. 175 (Suppl. 1), S183 – S188. Centers for Disease Control and Prevention, 1993. Progress toward global eradication of poliomyelitis, 1988 – 1991. MMWR Morb. Mort. Wkly Rep. 42, pp. 486–495. de Quadros, C.A., Hersch, B.S., Olive, J.M., Andrus, J.K., da Silveira, C.M., Carraso, P.A., 1997. Eradication of wild poliovirus from the Americas: acute flaccid paralysis surveillance, 1988 – 1995. J. Infect. Dis. 175 (Suppl. 1), S37– S42. Directorate General of Planning, 1998. Sultanate of Oman Health Facts. Ministry of Health, Sultanate of Oman. Dowdle, W.R., Featherstone, D.A., Birmingham, M.E., Hull, H.F., Aylward, R.B., 1999. Poliomyelitis eradication. Virus Res. 62, 185 – 192. Expanded Programme on Immunization, 1992. Serological and virological assessment of oral and inactivated poliovirus vaccines in a rural population. Wkly. Epidemiol. Rec. 67, pp. 179 – 182. Expanded Programme on Immunization, 1993. Poliomyelitis in 1992. Wkly. Epidemiol. Rec. 68, pp. 225 –230. Hull, H.F., Ward, N.A., Hull, B.P., Milstein, J.B., de Quadros, C., 1994. Paralytic poliomyelitis: seasoned strategies, disappearing disease. Lancet 343, 1331 –1337. Hull, B.P., Dowdle, W.R., 1997. Poliovirus surveillance: building the global polio laboratory network. J. Infect. Dis. 175 (Suppl. 1), S113 – S116. Hull, H.F., Birmingham, M.E., Melgard, B., Lee, J.W., 1997. Progress toward global polio eradication. J. Infect. Dis. 175 (Suppl. 1), S4 – S9. Jian, Z., Li-bi, Z., Otten, M.W., Tao, J., Xing-lu, Z., Rongzhen, Z., Ke-an, W., 1997. Surveillance for polio eradication in the Peoples Republic of China. J. Infect. Dis. 175 (Suppl. 1), S122 – S134. Ministry of Health, 1995. Progress toward poliomyelitis eradication –Oman: acute flaccid paralysis surveillance, 1990 –
1995. Community Health and Disease Surveillance Newsletter IV, pp. 1 – 5. Reichler, M.R., Kharabsheh, S., Rhodes, P., Otoum, H., Bloch, S., Majid, A.M., Pallansch, M.A., Patriarca, P.A., Cochi, S.L., 1997. Increased immunogenicity of oral poliovirus vaccine administered in mass vaccination campaigns compared with routine vaccination program in Jordan. J. Infect. Dis. 175 (Suppl 1), S198 – S204. Robertson, S.E., Suleiman, A.J.M., Mehta, F.R., Al-Dhahry, S.H.S., El-Bualy, M.S., 1994. Poliomyelitis in Oman: acute flaccid paralysis surveillance leading to early detection and rapid response to a type 3 outbreak. Bull. World Health Organ. 72, 907 – 914. Sutter, R.W., Patriarca, P.A., Brogan, S., Malankar, P.G., Pallansch, M.A., Kew, O.M., Bass, A.G., Cochi, S.L., Alexander, J.P., Hall, D.B., Suleiman, A.J.M., Al-Ghassany, A.A.K., El-Bualy, M.S., 1991. Outbreak of paralytic poliomyelitis in Oman: evidence for widespread transmission among fully vaccinated children. Lancet 338, 715 – 720. Wahdan, M.H., Aslanian, R., Reichler, M.R., Gafaar, M.T., 1997. Progress toward poliomyelitis eradication in the Eastern Mediterranean Region of the World Health Organization. J. Infect. Dis. 175 (Suppl. 1), S50 – S55. World Health Organization, 1988. Global eradication of poliomyelitis by the year 2000. Wkly. Epidemiol. Rec. 63, pp. 161 – 168. World Health Organization, 1992. Manual for the Virological Investigation of Poliomyelitis. Geneva. WHO/EPI/CDS/ POLIO 90.1. World Health Organization, 1999a. Progress towards poliomyelitis eradication, Nepal 1996 – 1999. Wkly. Epidemiol. Rec. 74, pp. 349 – 353. World Health Organization, 1999b. Progress towards poliomyelitis eradication, WHO Eastern Mediterranean Region. Wkly. Epidemiol. Rec. 74, pp. 405 – 408. World Health Organization. (1999c) Performance of acute flaccid paralysis surveillance and incidence of poliomyelitis, 1998 – 1999. Wkly. Epidemiol. Rec. 74, pp. 421 – 424. World Health Organization, 2000a. Global laboratory network for poliomyelitis eradication, 1997 – 1999: development and expanding contributions. Wkly. Epidemiol. Rec. 75, pp. 70 – 75. World Health Organization, 2000b. Performance of acute flaccid paralysis (AFP) surveillance and incidence of poliomyelitis, 1999 – 2000. Wkly. Epidemiol. Rec. 75, pp. 298 – 301.