Emerging Infectious Diseases Volume 19 Issue 9

2013·11.5 MB·English

by  CDC

Peer-Reviewed Journal Tracking and Analyzing Disease Trends pages 1361–1560
EDITOR-IN-CHIEF
D. Peter Drotman
Managing Senior Editor EDITORIAL BOARD
Polyxeni Potter, Atlanta, Georgia, USA
Dennis Alexander, Addlestone, Surrey, UK
Associate Editors Timothy Barrett, Atlanta, Georgia, USA
Paul Arguin, Atlanta, Georgia, USA Barry J. Beaty, Ft. Collins, Colorado, USA
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Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 19, No. 9, September 2013
September 2013
On the Cover Antigenic and Molecular
Characterization of Avian Infl uenza
Franconian painter of the
A(H9N2) Viruses, Bangladesh .........1393
Nuremberg School; active late
15th century in Nuremberg K. Shanmuganatham et al.
Reassortant trends in these viruses indicate the
The Miracle of Saint Vitus
(c. 1490) potential for transmission to mammalian hosts.
Oil on panel (116.8 cm x 99.1 cm)
Protection by Face Masks against
The John and Mable Ringling
Infl uenza A(H1N1)pdm09 Virus
Museum of Art, the State Art
Museum of Florida, a division of on Trans-Pacifi c Passenger Aircraft,
Florida State University 2009....................................................1403
About the Cover p. 1554 L. Zhang et al.
Comprehensive studies are needed to
Perspective assess this protective effect.
Podcast
Acute Encephalitis Syndrome
Surveillance, Kushinagar District,
Uttar Pradesh, India,
2011–2012 ..........................................1361 Mumps Postexposure
M. Kakkar et al. Prophylaxis with a
Low-quality data prevent informed policy Third Dose of Measles-
making and implementation of prevention and
Mumps-Rubella Vaccine,
control measures.
Orange County,
Synopses New York .........................1411
p. 1379
A. Parker Fiebelkorn et al.
Detection of Diphtheritic
Mumps attack rates were 0% among third
Polyneuropathy by Acute Flaccid
dose recipients and 5.2% among 2-dose
Paralysis Surveillance, India ...........1368
recipients who had not received postexposure
F.J. Mateen et al.
prophylaxis.
Throat examinations are useful in detecting
this disease.
Continued Evolution of West Nile Virus,
Houston, Texas, 2002–2012 ...............1418
Nodding Syndrome ..........................1374 p. 1390
B.R. Mann et al.
S.F. Dowell et al.
Ongoing surveillance is needed to better
Identifying the cause of this unexplained
understand transmission dynamics.
epidemic epilepsy is a major challenge.
Research
Underreporting of Viral Encephalitis
Divergent Astrovirus Associated with and Viral Meningitis, Ireland,
Neurologic Disease in Cattle ...........1385 2005–2008..........................................1428
L. Li et al. T.A. Kelly et al.
Cattle showing neurologic signs should be New case defi nitions and surveillance
tested for BoAstV-NeuroS1. modifi cations have been implemented to
capture omissions.
Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 19, No. 9, September 2013
Mycobacterium tuberculosis among September 2013
Socially Marginalized Immigrants in
Dispatches
Low-Incidence Area, Italy, 1991–2010
............................................................1437
1484 Microsporidial
I. Baussano et al.
Keratoconjunctivitis after Rugby
These populations may be responsible for Tournament, Singapore
substantial ongoing transmission and should be
J. Tan et al.
prioritized for screening.
1487 Novel Bunyavirus in Domestic
Plasmodium falciparum Mutant and Captive Farmed Animals,
Haplotype Infection during Pregnancy Minnesota
Associated with Reduced Birthweight, Z. Xing et al.
Tanzania ............................................1446
D.T.R. Minja et al.
1490 Benznidazole Treatment of
Suboptimal malaria treatments should urgently
Chagasic Encephalitis in
p. 1404
be replaced by screening and treatment with
Pregnant Woman with AIDS
safe and effective drugs.
M. Bisio et al.
New Estimates of Incidence of
1493 Mycobacterium chelonae
Encephalitis in England ...................1455
Abscesses Associated with
J. Granerod et al.
Biomesotherapy, Australia, 2008
Early recognition and accurate diagnosis of this M. Ivan et al.
disease are necessary to reduce economic and
societal costs.
1496 Spread of Neisseria meningitidis
Serogroup W Clone, China
Enzootic and Epizootic Rabies H. Zhou et al.
Associated with Vampire Bats,
Peru....................................................1463 p. 1494 1500 Human Parainfl uenza Virus
R.E. Condori-Condori et al.
Type 3 in Wild Nonhuman
Three putative new lineages were found in Primates, Zambia
hosts that may represent new reservoirs for
M. Sasaki et al.
this virus.
1504 Powassan Meningoencephalitis,
Staged Molecular Analysis to Determine
New York, New York
Causes of Unexplained Central Nervous
S. Sung et al.
System Infections .............................1470
C.-C. Hsu et al.
1507 Serogroup W135 Meningococcal
MassTag PCR may identify causes even
Disease, The Gambia, 2012
after other analyses have yielded negative
M.J. Hossain et al.
results.
Historical Review 1511 Novel Cyclovirus in Human
Cerebrospinal Fluid,
Quinto Tiberio Angelerio and New
Malawi, 2010–2011
Measures for Controlling Plague in
S.L. Smits et al.
16th-Century Alghero, Sardinia .......1478
R. Bianucci et al.
1514 Gastroenteritis Outbreak
Public health measures imposed by
Associated with Unpasteurized
Angelerio spared the surrounding areas from
Tempeh, North Carolina
the plague.
S.E. Griese et al.
Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 19, No. 9, September 2013
1540 Spread of Kyasanur Forest
Disease, Bandipur Tiger
September 2013 Reserve, India, 2012–2013
1518 West Nile Virus RNA in Tissues
1542 Chikungunya Virus Outbreak,
from Donor and Transmission
Brazzaville, Republic of Congo,
to Organ Transplant Recipients
2011
D.M. Blau et al.
1544 Chorea and Tick-borne
1521 R292K Substitution and Drug
Encephalitis, Poland
Susceptibility of Infl uenza
A(H7N9) Viruses
K. Sleeman et al. 1545 Streptococcus suis Meningitis
and Bacteremia in Man,
French Guiana
1525 Macrolide-Resistant
Mycoplasma pneumoniae in
Humans, Ontario, Canada, 1547 Alaria alata Infection in
2010–2011 p. 1544 European Mink
A. Eshaghi et al.
1549 Serologic Survey of Plague in
1528 Hepatitis E Virus Genotype 4, Animals, Western Iran
Nanjing, China, 2001–2011
X. Dai et al. 1551 Livestock Density as Risk
Factor for Livestock-associated
1531 Highly Pathogenic Avian MRSA, the Netherlands
Infl uenza A(H7N3) Virus in p. 1547 Book Review
Poultry Workers, Mexico, 2012
I. Lopez-Martinez et al. 1553 Neuroinfections
(What Do I Do Now?)
1535 Outbreak of Chikungunya Virus
Infection, Vanimo, Papua New
Guinea About the Cover
P.F. Horwood et al.
1554 When at night I go to sleep /
Letters
Fourteen angels watch do keep
1539 Clostridium diffi cile Infection
Etymologia
Caused by Binary Toxin–
Positive Strains 1553 Staphylococcus
Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 19, No. 9 September 2013
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ISBN-10: 0199315698 | ISBN-13: 978-0199315697
Acute Encephalitis Syndrome
Surveillance, Kushinagar District,
Uttar Pradesh, India, 2011–2012
Manish Kakkar, Elizabeth T. Rogawski, Syed Shahid Abbas, Sanjay Chaturvedi, Tapan N. Dhole,
Shaikh Shah Hossain, and Sampath K. Krishnan
In India, quality surveillance for acute encephalitis syn- the limitations of public health resources (1). However,
drome (AES), including laboratory testing, is necessary for identification of the etiologic agent is necessary for plan-
understanding the epidemiology and etiology of AES, plan- ning relevant interventions. The standard for determining
ning interventions, and developing policy. We reviewed AES the etiology of AES is examination of cerebrospinal fluid
surveillance data for January 2011–June 2012 from Kushi-
(CSF) during the acute phase of illness; pathogen-specific
nagar District, Uttar Pradesh, India. Data were cleaned, in-
IgM capture ELISA or nucleic acid amplification tech-
cidence was determined, and demographic characteristics
niques are used to detect pathogens in the CSF. Serologic
of cases and data quality were analyzed. A total of 812 AES
tests for pathogen-specific antibodies and virus detection
case records were identified, of which 23% had illogical en-
in serum are also recommended. However, examination of
tries. AES incidence was highest among boys <6 years of
age, and cases peaked during monsoon season. Records CSF is preferred because serologic test results may indi-
for laboratory results (available for Japanese encephalitis cate the presence of antibodies in the serum, but the AES
but not AES) and vaccination history were largely incom- may have a cause different than the agent producing the
plete, so inferences about the epidemiology and etiology detected antibodies (1–3).
of AES could not be made. The low-quality AES/Japanese A good quality surveillance system with laboratory
encephalitis surveillance data in this area provide little evi- support is essential for understanding the causes of AES
dence to support development of prevention and control
and responding appropriately. Accordingly, the National
measures, estimate the effect of interventions, and avoid
Vector Borne Diseases Control Programme in New Del-
the waste of public health resources.
hi, India, has developed guidelines for AES surveillance
that promote the need for a strong surveillance system as
Acute encephalitis syndrome (AES) is a clinical condi- a critical component for any control activities. In these
tion caused by infection with Japanese encephalitis guidelines, the goals outlined for AES surveillance are
virus (JEV) or other infectious and noninfectious causes. to 1) assess and characterize the burden of JE, 2) detect
A confirmed etiology is generally not required for the early warning signals for an outbreak, 3) assess the ef-
clinical management of AES. Thus, surveillance for JEV fect of vaccination, and 4) guide future strategies (1). The
infection in India has focused on identifying AES cases National Vector Borne Diseases Control Programme has
rather than JE cases; this approach is more feasible given also implemented several measures to strengthen local
health systems, including building on the capacity of the
Author affiliations: Public Health Foundation of India, New Delhi,
health workforce to provide better clinical management,
India (M. Kakkar, E.T. Rogawski, S.S. Abbas); University College
extending referral diagnostic facilities by upgrading the
of Medical Sciences, New Delhi (S. Chaturvedi); Sanjay Gandhi
existing Baba Raghav Das (BRD) Medical College facili-
Postgraduate Institute of Medical Sciences, Lucknow, India (T.N.
ties and setting up a National Institute of Virology field
Dhole); Centers for Disease Control and Prevention, New Delhi
unit; and establishing a dedicated surveillance unit in the
(S.S. Hossain); and Office of the World Health Organization Repre-
Department of Preventive and Social Medicine at BRD
sentative to India, New Delhi (S.K. Krishnan)
Medical College to provide improved surveillance and
DOI: http://dx.doi.org/10.3201/eid1909.121855 outbreak responses (4).
EEmmeerrggiinngg IInnffeeccttiioouuss DDiisseeaasseess •• wwwwww..ccddcc..ggoovv//eeiidd •• VVooll.. 1199,, NNoo.. 99,, SSeepptteemmbbeerr 22001133 1361
PERSPECTIVE
From the 1970s until around 2010, JEV infection was low numbers of AES cases so that sites could be select-
considered to be the leading cause of AES in the traditional ed for a larger study of the drivers of JEV transmission.
JE belt of India, which includes Kushinagar District in the Cases recorded in the line lists represented case-patients
state of Uttar Pradesh (5–11). However, because of a large from Kushinagar District who were 1) admitted directly
number of JE cases of unknown etiology, AES patterns to BRD Medical College, 2) referred to BRD Medical
alone have not suggested a clear picture of the epidemiol- College by the district hospital in Padrauna, and 3) admit-
ogy of the disease. In recent years, despite of the introduc- ted to the district hospital in Padrauna but had serum sam-
tion of a JE vaccine, an increased number of AES cases ples referred to BRD Medical College because no diagnos-
have been reported in India, including Uttar Pradesh, and tic kits were available and laboratory testing was limited
the disease has spread to new districts, urban areas, and at the district hospital. An individual AES patient tracking
villages without pigs, which are not usually associated with system does not exist in the state of Uttar Pradesh, so pa-
JE transmission (12,13). Thus, the assertion that JEV is the tients treated in the private sector or at the district hospital
leading cause of AES has been questioned, and other infec- in Gorakhpur were not included in the surveillance lists.
tious agents, such as enteroviruses, have been reported as
a cause of AES in Uttar Pradesh and other parts of India Preparation of Surveillance Database for Analysis
(14–19). A substantial contributor to the ambiguity about Individual identifiers for the case-patients were re-
the etiology of AES could be the fact that surveillance data moved from the line lists to ensure confidentiality. Data
for AES have not been analyzed to assess reasons for the were cleaned (i.e., extraneous data were removed) in mul-
increased cases and other reported causes. We examined tiple steps, resulting in 4 changes being made to the AES
the completeness and quality of AES surveillance data line lists. First, the spelling of residential localities (block,
from Kushinagar District, an area where JEV is highly en- village, or police station) were matched and standardized
demic. Herein, we discuss the ability to make inferences to result in a list of 32 residential areas. Residential areas
about AES epidemiology and etiology from these data and were then categorized and combined by block (14 blocks
the implications of our findings for policy planning and in Kushinagar). Modifications were validated by cross-
program implementation. checking with village population lists provided by Sav-
era, a local nongovernmental organization. Second, all
Methods age values were standardized to a uniform decimal sys-
tem (e.g., 1 year and 6 months was changed to 1.5 years,
Source of Surveillance Data and 8 months was changed to 0.67 year). Third, the dates
The sentinel site for JE surveillance in Kushinagar of symptom onset, hospital admission, sample collection,
District is the district hospital. Using a standard format, and outcome (i.e., discharged, left against medical advice,
the hospital reports all AES/JE cases that meet the standard or death) were standardized to 1 format. In the original
World Health Organization case definition (3) to the district list, dates were variously coded by using different nota-
malaria officer; this officer then forwards compiled data to tions (e.g., 4 March 2011 was mentioned within the same
the state program officer for transmission to National Vec- row as both 04/03/11 and 03/04/11). Assuming that the
tor Borne Disease Control Programme (http://nvbdcp.gov. case data were entered in chronological order, we stan-
in/Doc/AES%20guidelines.pdf). BRD Medical College in dardized dates by using, as a cue, the dates of the preced-
Gorakhpur, Uttar Pradesh, is a nearby regional field labo- ing and following AES cases. Fourth, case-patients who
ratory of the Indian Council of Medical Research, which died, were absent, or left against medical advice were
receives clinical samples from patients admitted to the dis- considered to have been discharged.
trict hospital in Kushinagar and completes most laboratory
testing for JEV infections. In addition, BRD Medical Col- Data Analysis
lege serves as a tertiary care center for patients who directly Cleaned data were imported into SAS version 9.2.2
seek medical care or who are referred from nearby districts, (SAS Institute, Inc., Cary, NC, USA) for analysis. AES
including Kushinagar. A line list with laboratory results of cases were plotted by week and month by using the re-
these patients is reported by BRD Medical College to the corded dates of symptom onset. We tabulated demographic
district malaria officer in Kushinagar for submission to characteristics of AES case-patients for 2011 and 2012
state program officers. and stratified case-patients by block, vaccination status,
In July 2012, we obtained the AES line lists data for laboratory test result for JEV infection, and clinical out-
January 2011–June 2012 that were submitted by BRD come. Incidence for 2011 was calculated by using popula-
Medical College to Kushinagar District Headquarters in tion denominators from the 2011 Census of India (20). We
Padrauna. The list was originally to be used to identify calculated incidence overall, by sex, and for children 0–6
blocks in Kushinagar District with high, medium, and years of age by using the age stratification available in the
1362 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 19, No. 9, September 2013
Acute Encephalitis Syndrome Surveillance, India

district-level census data. We estimated the incidence for
Table 1. Characteristics of case-patients with acute encephalitis
each block by using block-specific population denomina- syndrome, Kushinagar District, Uttar Pradesh, India, 2011–2012*
tors projected with the decadal growth rate from the 2001 No. (%) cases
Characteristic 2011, n = 721 2012, n = 91
Census of India (20). Crude incidence rate ratios were esti-
Age, y
mated with Wald-based CIs. 0–4 322 (44.7) 36 (39.6)
We also determined the median number of days be- 5–9 205 (28.4) 22 (24.2)
tween key points in AES disease progression and diagnosis: 10–14 83 (11.5) 12 (13.2)
15 111 (15.4) 21 (23.1)
time between onset of symptoms and hospital admission,
Sex
onset of symptoms and serum sample collection, hospital M 414 (57.4) 54 (59.3)
admission and serum sample collection, and hospital ad- F 307 (42.6) 37 (40.7)
Religion
mission and discharge or death. Using previously described
Hindu 632 (87.7) 80 (87.9)
methods (21), we evaluated the quality of the surveillance Muslim 89 (12.3) 11 (12.1)
data by assessing the amount of data cleaning required, Vaccinated against JEV
the proportion of missing or incomplete values in line list Yes 3 (0.4) 0
No 116 (16.1) 0
fields, and inconsistencies in dates recorded for key points
Unknown 602 (83.5) 91 (100)
in AES disease progression and diagnosis. Outcome
Died 130 (18.0) 18 (19.8)
Absent 18 (2.5) 0
Results
LAMA 16 (2.2) 0
Discharged 557 (77.3) 73 (80.2)
AES Epidemiology Result for JEV laboratory test
Positive 3 (0.4) 0
In 2011, a total of 721 AES cases from Kushinagar
Negative 128 (17.8) 0
District were identified through BRD Medical College; in
Awaited† 590 (81.8) 91 (100)
2012 (January–June), 91 cases were identified. Using the *Based on data obtained from Baba Raghav Das Medical College,
Gorakhpur, Uttar Pradesh, India. JEV, Japanese encephalitis virus; LAMA,
cleaned line lists, we determined the weekly number of
left against medical advice.
AES cases reported during January 2011–June 2012 (Fig- †Clinical samples awaiting laboratory test results.
ure 1). Cases peaked during August–October 2011; >150
cases were identified in each of these 3 months. This sea- Using 2011 population data (20), we estimated that
sonal trend corresponds with an expected increase in cases there were 20.2 AES cases/100,000 population in Kushi-
during the monsoon season, when transmission of both wa- nagar District in 2011 (Table 2). The incidence was higher
terborne and vector-borne diseases increases (vector den- among male residents than female residents (incidence rate
sity is at its maximum). ratio 1.29, 95% CI 1.11–1.49), and it was highest among
In 2011 and 2012, most case-patients were male children 0–6 years of age. The crude incidence rate ratio,
(57.4% and 59.3%, respectively) (Table 1). In 2011, al- comparing case-patients 0–6 years of age with those >6
most half of the AES cases were in children <5 years of years of age, was 7.97 (95% CI 6.87–9.25). Boys 0–6 years
age (44.7%); the distribution of cases by age group was not of age were at highest risk for AES. The incidence among
substantially different in 2012. The case-fatality rate was 0- to 6-year-old boys was almost 50% greater than that
18.0% in 2011 and 19.8% in 2012. among girls of the same age.
Figure 1. Weekly number of acute encephalitis syndrome cases, by month, in Kushinagar District, Uttar Pradesh State, India, 2011–2012.
Numbers are based on data obtained from Baba Raghav Das Medical College, Gorakhpur, Uttar Pradesh, India.
Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 19, No. 9, September 2013 1363
PERSPECTIVE
Table 2. Incidence of acute encephalitis syndrome, Kushinagar District, Uttar Pradesh, India, 2011–2012*
Age, sex of population 2011 population† No. cases Incidence‡ Incidence rate ratio (95% CI)
All ages 3,560,830 721 20.2
M 1,821,242 414 22.7 1.29 (1.11–1.49)
F 1,739,588 307 17.6 1.0
0–6 y 551,467 428 77.6
M 287,672 260 90.4 1.42 (1.17–1.72)
F 263,795 168 63.7 1.0
*Based on data obtained from Baba Raghav Das Medical College, Gorakhpur, Uttar Pradesh, India.
†From 2011 Census of India (20).
‡Per 100,000 population.

The weekly numbers of AES cases, classified by JE (i.e., awaiting determination) in the line lists for 82% (590)
IgM laboratory result (positive, negative, awaiting deter- of the 721 cases in 2011 and for all 91 cases in 2012 (Table
mination), is shown in Figure 2. Only 3 (4.2%) cases of 1). The line lists indicated the date of sample collection, but
JEV infection were identified in 2011: two cases were the type of sample collected (CSF and/or serum) and the
in 55-year-old men, 1 of whom died, and 1 case was in laboratory test used (IgM ELISA, PCR, and/or cell culture)
a 14-year-old girl. Vaccination status was reported for were not recorded for any of the case-patients. Most sam-
119 case-patients, of whom 3 (2.6%) had been vaccinated. ples submitted after July 2011 were still awaiting labora-
The case-patients who had received vaccine were boys tory results at the time of our study (Figure 2). In addition,
6, 7, and 8 years of age; they began experiencing symp- for 602 (83.5%) of the 721 case-patients in 2011 and all 91
toms in July 2011 and were discharged within 3 weeks case-patients in 2012, JEV vaccination status was marked
of hospital admission. None of the 3 JE case-patients had as “unknown” in the line lists (Table 1).
been vaccinated. Key epidemiologic and programmatic indicators, such
as the time between key points in AES disease progression
Quality of Surveillance Data and diagnosis, varied widely among case-patients (Table
During data cleaning, we modified 25% of the 2011 4). In some instances, the dates were illogical (e.g., dates of
and 5% of the 2012 line list values for residential locality, symptom onset and sample collection following and pre-
age, and date parameters (Table 3). Nearly one fifth of the ceding the dates of hospital admission, respectively). It was
age data and more than one fourth of the dates were edited. not possible to rectify these inconsistencies on the basis of
For 3.2% and 13.2% of cases in 2011 and 2012, respective- the available data. In addition, the range of values was of-
ly, the block name could not be determined from the resi- ten large. For example, median time from onset of symp-
dential locality provided and was marked as “unknown” toms to hospital admission was 4 days in 2012, but some
because the village or police station name was not found or patients were admitted >2 months after symptom onset.
was present in multiple blocks. In addition, several fields in Because AES is an acute syndrome, a long interval is not
the database were incomplete. As of July 2012, laboratory expected between symptoms and may indicate reporting of
results for JEV infection were still classified as “awaited” unrelated symptoms or misclassification of AES.
Figure 2. Weekly number of acute
encephalitis syndrome cases, by
month, in Kushinagar District,
Uttar Pradesh State, India,
2011–2012. Numbers represent
results of laboratory testing for
Japanese encephalitis and are
based on data from Baba Raghav
Das Medical College, Gorakhpur,
India. In the key, “awaited” refers
to samples that were awaiting
laboratory test results.
1364 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 19, No. 9, September 2013