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Ind

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IND- Definitief

Genetic variants of echovirus 13, northern India, 2010.

Although polio has not been reported from India since January 2011,
spurts in the rate of nonpolio acute flaccid paralysis (AFP) are of
concern. Therefore, other viral agents associated with AFP need to be
identified, especially nonpolio human enteroviruses (HEVs), which are a
major cause of neurologic illness.

The classic method for HEV serotypic identification requires virus
isolation in susceptible cell cultures, followed by virus neutralization
tests. However, the procedure is laborious, slow, and incapable of
identifying new serotypes for which no reference antiserum is available
(1). Nonpolio HEV typing based on viral protein (VP) 1 sequences has
been developed and correlates well with antigenically defined serotypes
(2).

Since 1998, we have been actively involved in polio surveillance
and passively reporting nonpolio HEV activity in Uttar Pradesh State,
northern India. Most nonpolio HEVs were isolated during the
summer-autumn season and identified by using methods based on antigenic
serotyping (3). We used a method combining a single cell culture passage
with VP1 reverse transcription PCR (RT-PCR) and sequencing for rapid
identification of nonpolio HEV serotypes. The predominant nonpolio HEV
found was echovirus (E) 13, a serotype rarely isolated in India.

The Study

Nonpolio AFP case-patients showing signs of acute onset of focal
weakness or paralysis characterized as flaccid (reduced muscle tone) and
preceded by fever were considered for NPEV analysis. A total of 347
fecal specimens collected in Uttar Pradesh during March-August 2010 from
children <15 years of age who had AFP symptoms were analyzed by using
a modified World Health Organization (WHO) method (4,5).

Fecal specimens were processed according to the WHO protocol (4).
Human rhabdomyosarcoma and L20B (mouse fibroblast cells expressing the
poliovirus receptor) cell lines used for virus isolation were observed
for cytopathic effect (CPE). The positive isolates with enterovirus
(EV)-like CPE were tested by using pan-poliovirus and pan-EV RT-PCR (4).
All poliovirus isolates characterized according to WHO algorithm were
excluded from the analysis presented here. Viral RNA was extracted from
the first-pass rhabdomyosarcoma cell suspension with the Viral RNA Mini
Kit (QIAamp, QIAGEN, Hilden, Germany). Genotyping was done by RT-PCR of
a portion of the VP1 gene and sequencing as described (2,6).

MEGA version 5.05 software (7) was used for phylogenetic analysis.
Distance matrices of the nucleotide and amino acid sequences were
analyzed with the MegAlign program in the Lasergene software package
(DNASTAR, Madison, WI, USA).

Of 347 fecal samples analyzed, 73 (21%) cell cultures tested
positive by pan-EV 5' nontranslated region RT-PCR. Nineteen (5%)
were pan-poliovirus positive, leaving 54 (16%) nonpolio HEVs for
analysis. Genotyping of 45 (83%) EVs by partial VP1 sequencing followed
the criteria of Oberste et al. (2). CPE was observed in rhabdomyosarcoma
cells in the first passage for 33 samples, of which 27 were pan-EV
positive, identified as E13 (21 [64%]), E7 (2 [6%]), E4 (1 [3%]), E33 (1
[3%]), and EV75 (2 [6%]); 6 isolates remained untypeable. Of the 21
samples that did not yield CPE in rhabdomyosarcoma cells in the first
passage, 18 were pan-EV positive, identified as E25 (4 [19%]), E13 (9
[43%]), coxsackievirus B3 (CVB3; 3 [14%]), CVB6 (2 [10%]). Three
isolates could not be identified because of poor quality sequence data.

E13 was the most common nonpolio HEV identified. Because E13 has
rarely been isolated in India, we analyzed the Uttar Pradesh E13
isolates for March-August 2010 from 5 adjoining districts of western
Uttar Pradesh (Lakhimpur-Kheri, Sitapur, Lucknow, Raebareli, and
Hardoi). Clinical findings (Table 1) showed that 20 (67%) of the 30
patients had asymmetric paralysis at onset, including 3 AFP
case-patients with fever at onset of paralysis and residual paralysis
mimicking poliolike illness; however, when compared with other
etiologies, no conclusion was inferred (Table 2).

The 244-nt partial VP1 gene sequence of all the Uttar Pradesh E13
isolates shared 75.4%-79.9% nt identity and 87.7%-93.8% aa identity with
the prototype EV13 strain, Del Carmen (GenBank accession no. AY302539).
Phylogenetic analysis indicated the existence of 2 different Uttar
Pradesh E13 clades in the neighbor-joining tree (Figure). Uttar Pradesh
2010 E13 viruses in the largest clade segregated into 3 groups (labeled
A-C, Figure), whereas the second large 2010 Uttar Pradesh E13 clade was
monophyletic (labeled D, Figure). Partial VP1 sequences of Uttar Pradesh
E13 clade A shared 96.5%-100% nt identity (100% aa identity) with one
another. Clade B shared 89.4%-90.7% nt identity (95.5%-98.8% aa
identity) with clade A and 84.2%-84.5% nt identity (97.5% aa identity)
with clade C. Clade C shared 88.9%-88.1% nt identity (95.5%-98.8% aa
identity) with clade A. Uttar Pradesh E13 clade D shared 73%-76% nt
identity (90.1%-93.5% aa identity) with clades A, B, and C. Although
variation exists among the partial VP1 sequences of E13 strains from
India, the E13 clades A, B, and C appear to be closely related to
earlier India isolates (2007 and 2008) followed by the isolates from
Pakistan (2009), Bangladesh (2000), and the Republic of Georgia (2004).
The E13 D clade was genetically more distant and grouped together with
year 2000 strains from India and Bangladesh (isolated in 1999), and 1
isolate from Georgia (isolated in 2004).

Conclusions

We demonstrated the utility of a modified WHO laboratory protocol
by combining classical and molecular methods for rapid detection and
identification of nonpolio HEV (2,4-6). Identifying the EV in mixed EV
infections is challenging when this protocol is used, but on balance,
pan-EV testing followed by VP1 RT-PCR and sequencing delivers rapid
results and more efficient use of labor and resources than does the
traditional method and enables identification of newer EV types.

Numerous reports have described AFP patients infected with EVs,
coxsackieviruses, and newer numbered EVs (3,8). Nonpolio HEVs also have
been detected in epidemics of paralytic disease (9). Although nonpolio
HEVs can be isolated from asymptomatic children, few studies have
compared the nonpolio HEV serotypes found in AFP case-patients and in
healthy children. Identifying nonpolio HEV serotypes associated with AFP
in India provides useful EV surveillance data and should be explored
further in conjunction with virologic evaluation of appropriate
community controls and additional clinical specimens from AFP
case-patients (cerebrospinal fluid, throat swab samples, serum), which
could indicate the nonpolio HEV type causing paralytic disease.

[FIGURE OMITTED]

We identified 8 nonpolio HEV serotypes (E4, E7, E13, E25, E33,
EV75, CVB3, and CVB6). E13, the predominant serotype, has been isolated
rarely (3,10); however, nonpolio HEVs have been reported from India in
connection with sporadic and epidemic meningitis/encephalitis cases
(11,12). A wide spectrum of illnesses have been reported with E13 (13),
so finding E13-associated AFP cases mimicking poliomyelitis (14) is not
surprising.

The global aseptic meningitis epidemic caused by E13 during
2000-2003 was associated with a single E13 genotype (15); however, our
findings indicate that several different and genetically diverse E13s
have been cocirculating in India. The Uttar Pradesh E13 partial VP1 gene
sequences are most closely related to recent E13 strains from central
and southern Asia. The high genetic diversity among the Uttar Pradesh
E13 isolated from patients in a local area over 6 months implies a
continuous pattern of circulation. High-density human populations,
immunologically susceptible cohorts, and nonhygienic environmental
conditions probably facilitated the E13 genetic heterogeneity in our
study.

Although we report a high prevalence of E13 infection in AFP
case-patients, our study is restricted by the modest number of cases
from a small geographic area sampled over a short period. The
epidemiologic and nonpolio HEV genetic information gathered warrants
further studies in larger groups of children to gain better insight into
AFP caused by nonpolio HEV and to identify the etiologic nonpolio HEV
type(s) associated with sporadic or epidemic AFP as India nears the goal
of polio elimination.

Acknowledgments

We thank the WHO Regional Polio Reference Laboratory at Sanjay
Gandhi Postgraduate Institute of Medical Sciences, Lucknow, for AFP
samples; and William Allan Nix for technical discussion and useful
suggestions in the manuscript.

This work was supported by a grant-in-aid from the Indian Council
of Medical Research, Ministry of Health and Family Welfare, Government
of India, New Delhi, India (grant no. 3/1/ JRF/69/MPD-2006 to H.S. M.).

Mr Maan is a research student at Sanjay Gandhi Postgraduate
Institute of Medical Sciences. His research interests include the
molecular detection and epidemiology of enteroviruses and emerging viral
infections associated with AFP.

References

(1.) Oberste MS, Maher K, Flemister MR, Marchetti G, Kilpatrick DR,
Pallansch MA. Comparison of classic and molecular approaches for the
identification of untypeable enteroviruses. J Clin Microbiol.
2000;38:1170-4.

(2.) Oberste MS, Maher K, Kilpatrick DR, Pallansch MA. Molecular
evolution of the human enteroviruses: correlation of serotype with VP1
sequence and application to picornavirus classification. J Virol.
1999;73:1941-8.

(3.) Dhole TN, Ayyagari A, Chowdhary R, Shakya A, Shrivastav N,
Datta T, et al. Non-polio enteroviruses in acute flaccid paralysis
children of India: vital assessment before polio eradication. J Paediatr
Child Health. 2009;45:409-13. http://dx.doi.org/10.1111/
j.1440-1754.2009.01529.x

(4.) World Health Organization. Polio laboratory manual. 4th ed.
Geneva: The Organization; 2004.

(5.) Dias AP, Tavares FN, Costa EV, da Silva EE. Evaluation of a
protocol for rapid diagnosis of enterovirus associated with acute
flaccid paralysis cases. J Clin Virol. 2009;46:337-40. http://dx.doi.
org/10.1016/j.jcv.2009.09.008

(6.) Oberste MS, Nix WA, Maher K, Pallansch MA. Improved molecular
identification of enteroviruses by RT-PCR and amplicon sequencing. J
Clin Virol. 2003;26:375-7.

http://dx.doi.org/10.1016/S138-66532(03)00004-0

(7.) Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S.
MEGA5: Molecular Evolutionary Genetics Analysis using maximum
likelihood, evolutionary distance, and maximum parsimony methods. Mol
Biol Evol. 2011;28:2731-9. http://dx.doi. org/10.1093/molbev/msr121

(8.) Junttila N, Leveque N, Kabue JP, Cartet G, Mushiya F,
Muyembe-Tamfum JJ, et al. New enteroviruses, EV-93 and EV-94, associated
with acute flaccid paralysis in the Democratic Republic of the Congo. J
Med Virol. 2007;79:393-400. http://dx.doi.org/10.1002/ jmv.20825

(9.) Perez-Velez CM, Anderson MS, Robinson CC, McFarland EJ, Nix
WA, Pallansch MA, et al. Outbreak of neurologic enterovirus type 71
disease: a diagnostic challenge. Clin Infect Dis. 2007;45:950-7.

http://dx.doi.org/10.1086/521895

(10.) Khetsuriani N, Kutateladze T, Zangaladze E, Shutkova T,
Penaranda S, Nix WA, et al. High degree of genetic diversity of
non-polio enteroviruses identified in Georgia by environmental and
clinical surveillance, 2002-2005. J Med Microbiol. 2010;59:1340-7.
http:// dx.doi.org/10.1099/jmm.0.023028-0

(11.) Kumar A, Shukla D, Kumar R, Idris MZ, Misra UK, Dhole TN. An
epidemic of encephalitis associated with human enterovirus B in Uttar
Pradesh, India, 2008. J Clin Virol. 2011;51:142-5. http://
dx.doi.org/10.1016/j.jcv.2011.02.011

(12.) Kumar A, Shukla D, Kumar R, Idris MZ, Jauhari P, Srivastava
S, et al. Molecular identification of enteroviruses associated with
aseptic meningitis in children from India. Arch Virol. 2012; Epub ahead
of print. http://dx.doi.org/10.1007/s00705-012-1476-7

(13.) Kobayashi K, Haruta T, Kubota M, Akiyoshi K, Suga T, Ito M.
Clinical spectrum in hospitalized children with echovirus type 13
infection. Pediatr Int. 2005;47:185-9. http://dx.doi.org/10.1111/
j.1442-200x.2005.02046.x

(14.) Apostol LN, Suzuki A, Bautista A, Galang H, Paladin FJ, Fuji
N, et al. Detection of non-polio enteroviruses from 17 years of
virological surveillance of acute flaccid paralysis in the Philippines.
J Med Virol. 2012;84:624-31. http://dx.doi.org/10.1002/jmv.23242

(15.) Mullins JA, Khetsuriani N, Nix WA, Oberste MS, LaMonte A,
Kilpatrick DR, et al. Emergence of echovirus type 13 as a prominent
enterovirus. Clin Infect Dis. 2004;38:70-7. http://dx.doi.
org/10.1086/380462

Harjeet Singh Maan, Rashmi Chowdhary, Akhalesh Kumar Shakya, and
Tapan N. Dhole

Author affiliations: Sanjay Gandhi Postgraduate Institute of
Medical Sciences, Lucknow, India (H.S. Maan, A.K. Shakya, T.N. Dhole);
and Columbia University, New York, New York, USA (R. Chowdhary)

DOI: http://dx.doi.org/10.3201/eid1902.111832

Address for correspondence: Tapan N. Dhole, Department of
Microbiology, Sanjay Gandhi Postgraduate Institute of Medical Sciences,
Raebareli Rd, Lucknow-226010, Uttar Pradesh, India; email:
tapandhole321@yahoo.in

Table 1. Clinical and virologic findings for AFP case-patients from
whom echovirus 13 was isolated, Uttar Pradesh, India, 2010 *

Clade,([dagger]) isolate      Month        District      Patient age,
name ([double dagger])     ([section])   ([paragraph])      y/sex

A

Har01/IND/UP/Echo13/2010       Mar            LNO           3.10/M
Har05/IND/UP/Echo13/2010       Mar            STP           2.9/F
IND-29-2010                    Mar            LNO           4.4/F
IND-30-2010                    Mar            LNO           6.0/M
IND-34-2010                    Mar            KRI           8.0/M
IND-35-2010                    Mar            STP           1.5/M
IND-36-2010                    Mar            STP           4.0/M
IND-43-2010                    May            LNO           2.5/M
IND-37-2010                    May            STP           2.3/F
IND-38-2010                    May            STP           2.8/M
IND-42-2010                    May            STP           4.7/M
IND-45-2010                    May            STP           9.0/M
IND-20-2010                    Aug            KRI           4.0/M
IND-21-2010                    Aug            KRI           8.0/M
IND-12-2010                    Apr            KRI           0.9/F
IND-17-2010                    Apr            KRI           2.0/M

B

IND-23-2010                    Jul            HDO           2.0/F
IND-24-2010                    Jul            HDO           2.5/M

C

IND-14-2010                    Jul            KRI           1.4/M
IND-16-2010                    Jul            KRI           2.0/M
IND-19-2010                    Jul            KRI           2.5/F
IND-18-2010                    Jul            KRI           3.0/F

D

IND-15-2010                    Jul            KRI           6.5/M
IND-22-2010                    Aug            HDO           4.5/M
IND-40-2010                    Aug            RBL           2.0/M
IND-39-2010                    Aug            LNO           4.0/F
IND-41-2010                    Aug            LNO           4.5/M
IND-44-2010                    Aug            LNO           3.0/M
IND-33-2010                    Aug            HDO           2.0/F
IND-32-2010                    Aug            HDO           2.0/M

Clade,([dagger]) isolate     Disease onset       Paralysis status
name ([double dagger])                             after 60-day
                                                follow-up (residual
                                                    paralysis)

                           Fever   Asymmetric
                                   paralysis

A

Har01/IND/UP/Echo13/2010                                 +
Har05/IND/UP/Echo13/2010     -         -                 +
IND-29-2010                  -         -                 -
IND-30-2010                  -         -                 -
IND-34-2010                  -         +                 -
IND-35-2010                  +         +                 -
IND-36-2010                  +         -                 -
IND-43-2010                  +         +                 -
IND-37-2010                  -         +                 -
IND-38-2010                  +         +                 -
IND-42-2010                  -         -                 +
IND-45-2010                  -         +                 -
IND-20-2010                  +         +                 -
IND-21-2010                  -         -                 -
IND-12-2010                  +         +                 -
IND-17-2010                  -         +                 -

B

IND-23-2010                  +         +                 +
IND-24-2010                  +         +                 -

C

IND-14-2010                  +         +
IND-16-2010                  +         +                 -
IND-19-2010                  +         +                 -
IND-18-2010                  -         +                 -

D

IND-15-2010                  +         +                 +
IND-22-2010                  -         -                 -
IND-40-2010                  -         -                 -
IND-39-2010                  -         +                 -
IND-41-2010                  +         -                 +
IND-44-2010                  +         +                 -
IND-33-2010                  +         +                 +
IND-32-2010                  -         +                 -

* AFP, acute flacid paralysis; LNO, Lucknow; S IP, Sitapur;
KRI, Lakhimpur-Kheri; HDO, Hardoi; RBL, Raebareli; - absence
of clinical feature; + presence of clinical feature.

([dagger]) Different clades (Figure) of echovirus 13 identified
in the study.

([double dagger]) Designation of investigated isolates of all
Uttar Pradesh 2010 echovirus 13 isolates.

([section]) Month of isolation.

([paragraph]) District of AFP patient.

Table 2. Clinical characteristics of 45 AFP case-patients with
nonpolio enterovirus serotypes, Uttar Pradesh, India, 2010 *

Sign/symptom                  AFP case-patients with serotype, no. (%)

                               E13,      E25,     E7,       E4,
                              n = 30    n = 4    n = 2     n = 1

Fever at onset of paralysis   15 (50)   3 (75)     -        -
Asymmetric paralysis          20 (67)   2 (50)   1 (50)   1 (100)
Residual paralysis            7 (23)      -        -      1 (100)

Sign/symptom                  AFP case-patients with serotype, no. (%)

                               E33,      EV75,     CVB6,     CVB3,
                               n = 1     n = 2     n = 2     n = 3

Fever at onset of paralysis   1 (100)   2 (100)     -       3 (100)
Asymmetric paralysis            -       2 (100)   2 (100)   2 (67)
Residual paralysis              -       1 (50)      -         -

* AFP, acute flacid paralysis, E, echovirus; EV, enterovirus;
CVB, coxsackievrius B; -, absence of clinical feature.

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