Volume 14, Issue 22 - 4 June 2009

Transcript

Volume 14, Issue 22 - 4 June 2009
Rapid communications
Transmission potential of the new influenza A(H1N1) virus and its age-specificity in Japan
2
by H Nishiura, C Castillo-Chavez, M Safan, G Chowell
Epidemiology of new influenza A (H1N1) virus infection, United Kingdom, April – June 2009 6
by Health Protection Agency, Health Protection Scotland, National Public Health Service for Wales, HPA Northern Ireland
Swine influenza investigation teams
Evaluation of four real-time PCR assays for detection of influenza A(H1N1)v viruses 9
by J Ellis, M Iturriza, R Allan, A Bermingham, K Brown, J Gray, D Brown
Origins of the new influenza A(H1N1) virus: time to take action
12
by GM Nava, MS Attene-Ramos, JK Ang, M Escorcia
Norwegians approve of the health authorities’ strategy to communicate worst case pandemic scenarios
37
by G Wøien, KI Tonsberg
Research articles
Autochthonous cystic echinococcosis in patients who grew up in Germany
by J Richter, A Orhun, B Grüner, I Müller-Stöver, S Reuter, T Romig, D Häussinger, P Kern
EUROPEAN CENTRE FOR
DISEASE PREVENTION
AND CONTROL
39
R a p i d c o m m u n i c a ti o n s
Transmission
p ot e n t i a l o f t h e n e w i n f l u e n z a
v i r u s a n d i t s a g e - s p e c i f i c i t y i n J a pa n
A(H1N1)
H Nishiura ([email protected])1, C Castillo-Chavez2, M Safan3, G Chowell2
1.University of Utrecht, Utrecht, the Netherlands
2.Arizona State University, Tempe, Arizona, United States
3.Mansoura University, Mansoura, Eg ypt
On 16 May 2009, Japan confirmed its first three cases of new
influenza A(H1N1) virus infection without a history of overseas
travel, and by 1 June, 361 cases, owing to indigenous secondary
transmission, have been confirmed. Of these, 287 cases (79.5%)
were teenagers (i.e. between 10 and 19 years of age). The
reproduction number is estimated at 2.3 (95% confidence interval:
2.0, 2.6). The average number of secondary transmissions involving
minors (those under 20 years of age) traced back to infected minors
is estimated at 2.8. That is, minors can sustain transmission even
in the absence of adults. Estimates of the effective reproduction
number Rt moved below 1 by 17 May. Active surveillance and
public health interventions, including school closures most likely
have contributed to keeping Rt below one.
Introduction
The reproduction number R, the average number of secondary
cases generated by a single primary case, of the new influenza
A(H1N1) virus, is a key quantitative measure for assessing
pandemic potential [1]. In the ongoing epidemic of the new
influenza A(H1N1) virus, early studies suggested that R ranged
from 1.4-1.6 [2] and some estimated it to be as high as 2.2-3.1
[3]. Estimates in 1.4-1.6 range for the new influenza A(H1N1)
virus are lower than estimates based on data from, for example,
the fall wave of the 1918 influenza pandemic [4,5]. The present
study investigates indigenous secondary transmissions of the new
influenza A(H1N1) virus in Japan, not only estimating R but also
exploring its age-specificity.
worker at Tokyo-Narita airport) [6]. Figure 1 shows the geographic
distribution of 361 indigenous cases. Cases outside Osaka and
Hyogo prefectures had travel histories to Osaka or Hyogo before
their illness onset. The index case(s) (who may have remained
asymptomatic [7]), with a history of overseas travel, has (have)
yet to be identified. Furthermore, there are no known cases prior
to the five confirmed cases that developed the disease on 9 May
in Hyogo (Figure 2A). The triggering event may be associated with
Japan’s two-week festive break, the “golden week”, just before 9
May, when people may have travelled to and returned from Mexico,
United States and Canada.
Figure 1
Spatial distribution of the epidemic of new influenza
A(H1N1) virus infection in Japan. Cumulative number of
confirmed indigenous cases, as of 1 June 2009 (n = 361)
Methods
Epidemiological description of the epidemic
On 16 May 2009, three high school students in Kobe city, Hyogo
prefecture, without a history of overseas travel, were confirmed
as infected with the new influenza A(H1N1) virus. Confirmatory
diagnosis in Japan requires influenza-like symptoms and a laboratory
diagnosis which is made either by virus isolation, real-time PCR
or a significant increase in neutralising antibody titre against the
virus. Further confirmed diagnoses followed predominantly in
Hyogo and Osaka prefectures. The increased number of infections
among particular age groups was most evident in the data from
prefectures where most secondary cases were found among high
school students attending different schools.
By 1 June, the Ministry of Health, Labour and Welfare of Japan
had reported 371 confirmed cases, including nine imported cases
and one case traced back to a distant international airport (i.e. a
2
Note: Cases in Tokyo, Saitama, Shiga and Kyoto had travel history to either
Hyogo or Osaka prefecture before illness onset. Kobe city, where first
three cases were diagnosed, is a capital city of Hyogo prefecture.
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We analysed the temporal incidence distribution of confirmed
cases for this epidemic (Figure 2A). The known dates of illness
onset are used except for a fraction of the confirmed cases in Kobe
city (45; 12.5%) whose dates of onset have yet to be fully clarified.
Since the known median time from onset to diagnosis in Kobe
has been estimated at 1.0 day [8], it is assumed that the dates of
onset among the 45 cases in Kobe were 1 day before their date of
diagnosis. We observed that by the time the first three cases had
been confirmed (16 May), the epidemic curve was just about at its
peak. 16-17 May fell on a weekend, and all schools in Osaka and
Hyogo were officially closed for one week starting on 18 May. Figure
2B displays the age-distribution of the 361 confirmed cases, which
is concentrated in the teenage population. We see the age-specific
window (10-19 years of age) that includes 287 confirmed cases
(79.5%; 95% confidence interval (CI): 75.3, 83.7).
Epidemiological analysis
Taking into consideration the high levels of uncertainty related
to the invasion of a population by a novel influenza virus, three
different methods are used to estimate the transmission potential
of the new influenza A(H1N1) virus. To concentrate on the
transmission potential in Japan, all nine imported cases and one
case that is not associated with indigenous transmission in Hyogo
and Osaka were removed from the following analyses.
Model 1 (M1)
Estimation of R using the intrinsic growth rate [3,5]. The
intrinsic growth rate r, is estimated via a pure birth process [9].
The likelihood is proportional to:
(
)
exp − r ∑ i = 0 C ( i ) (1 − exp ( − r ) )
t −1
C ( t ) − C ( 0)
where C(t) denotes the cumulative number of cases on day
t. C(0) = 5 and t = 0 represents 9 May. The generation time (GT) is
assumed to follow a gamma distribution with mean μ= 1.9 days and
coefficient of variation ν = 47% [2]. R is subsequently estimated
using the estimator [10]:
1
2 v2
(1 + r µ v )
Given that many serial intervals reported from Spain are longer
than 1.9 days [7], the uncertainties surrounding GT estimates are
partially addressed through a sensitivity analysis of R to variations
in the mean GT in the range from 1.3-4.0 days. The exponential
growth phase is assumed to have a mean duration of 8 days but
windows in the 8±2 days were also used.
Model 2 (M2)
The effective reproduction number Rt, the average number of
secondary cases generated by a primary case at time t, is estimated.
The daily growth rate rt is used to estimate Rt following the approach
described elsewhere [11]; the distribution of GT and the estimator
of R used are the same as those used in M1. The mean GT is
assumed to be 1.9 days but varying in the 1.3 to 2.5 days range [2].
Figure 2
Time- and age-specificity of the epidemic of new influenza A(H1N1) virus infection in Japan
A) Epidemic curve of confirmed indigenous cases according to the date of illness onset, as of 1 June 2009 (n = 361)
B) Age distribution of confirmed indigenous cases, as of 1 June 2009 (n=361)
A
B
C
360
20
180
120
10
60
0
0
27
10-19
0-9
29-May
27-May
25-May
23-May
21-May
19-May
17-May
15-May
13-May
11-May
9-May
7-May
15
11
13
5
3
60 and
older
30
240
50-59
40
40-49
Confirmed cases
50
287
300
30-39
Age group
20 and older
0-19
60
Confirmed cases
B
20-29
A
70
Age (years)
Note: None of the confirmed cases had recent history of overseas travel (except for one case in Wakayama). The nine cases, believed to have become
infected abroad, and one case, arising in a worker at Tokyo-Narita airport, are excluded from these figures.
The dates of illness onset for each confirmed case are reported by prefectural governments, except for a fraction of cases in Kobe city where cases with
unknown dates of onset are assumed to have developed the disease one day before the confirmatory diagnosis (based on published median estimate [8]).
It should be noted that the dates of onset are based on preliminary reports and have yet to be refined.
Arrow A indicates the date on which the first three cases were diagnosed in Kobe city. All schools in Hyogo and Osaka were closed between the dates
signalled by the arrows B and C.
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Model 3 (M3)
The role of age-specificity in transmission is analysed using
estimates of the next-generation matrix, K (Figure 3). First, we
aggregate the population in two age groups, minors and adults.
Second, since the mean GT is approximately 2 days [2], the daily
number of cases during the exponential growth phase (i.e. first
8 days) uses as its unit of time, two-day intervals (i.e. cases, c,
in days 1 & 2, 3 & 4, 5& 6 and 7 & 8 are grouped). Third, the
expected value of cases in age-group i of grouped-generation τ,
E(ci(τ)), is modelled by Riici(τ-1)+Rijcj(τ-1) (fort = 2, 3 and 4) where
Rgh is the element of K that corresponds to the average number
of secondary cases in group g caused by an infected individual in
group h. We estimate the entries in the matrices, assuming two
different mixing patterns modelled via two unknown parameters by
means of Poisson regression (Figure 3).
Results
The intrinsic growth rate r, is estimated at 0.47 (0.40, 0.56) per
day. Accordingly, M1 gives an R estimate of 2.3 (95% CI: 2.0, 2.6).
Figure 4A illustrates the sensitivity of R to variations in the mean
GT in the range 1.3-4.0 days. The corresponding R estimates lie
in the 1.8 to 4.8 range. Variations in the initial growth phase (i.e.
±2 days) do not greatly influence R; i.e. the expected values of R
lie in the 1.9 to 2.3 range. The exclusion of the less documented
cases in Kobe lead to an R estimate of 2.0 (95% CI: 1.7, 2.3).
Use of M2 suggests that Rt peaked on 14 May (Figure 4B). On
17 May, the day after a press release announced the first three
confirmed diagnoses, Rt declined below 1. Under active surveillance
efforts and school closures, Rt was kept below 1 thereafter.
Consistent temporal patterns of Rt are seen using different values,
except for slight increase and decrease in Rt estimates, for GT mean
values in the 1.3-2.5 day-range.
Figure 3
Next-generation matrix
Using M3, the next-generation matrix, K1 estimate, under the
separable mixing assumption is
 2.82 0.32 
Kˆ 1 = 

 0.32 0.04 
while our K2 estimate based on a qualitative assumption of
WAIFW (who acquired infection from whom) matrix is
 2.82 0.29 
Kˆ 2 = 

 0.29 0.29 
The host-specific reproduction number [12] for minor, i.e. the
average number of secondary minor cases generated by a single
primary minor case was 2.8 under K1 and K2. Hence a population
of minors can sustain the chains of secondary transmission even in
the absence of adults (i.e. for this epidemic “minors” are the “core”
group). Our estimate of R based on M3 is the largest eigenvalue
of K, and R is estimated at 2.9 for both matrices. These estimates
are slightly greater than R estimates based on M1; when the mean
and variance of GT is 2.0 days and 0 days2 (i.e. if GT is constant,
following a delta function), our R estimate is 2.6.
Discussion
Two important conclusions can be drawn from our epidemiological
analyses. Firstly, the reproduction number R of the new influenza
A(H1N1) virus in Japan is estimated to be as high as 2.3, a value
that is significantly higher than that recently reported [2]. The
pandemic potential of this virus in Japan may be higher in terms of
transmission potential than in other areas of the world. In particular,
it should be noted that our estimate of R is greater than published
estimates for seasonal influenza epidemics in temperate countries
[13]. Given that our R estimate has been tested for robustness to
uncertainty to mean GT, it seems plausible that high contact rates
among teenagers (when compared to other populations) may be one
of the main drivers of this epidemic. From a transient increase in
Rt around 14 May, our high estimate of R may reflect the existence
of few highly connected clusters of cases among “cliques” of high
school students. There may be additional contributing factors to
variations in our R estimates, including cross-protective immunity
due to previous exposure to other closely related influenza viruses.
Secondly, our age-specific estimates support the view that minors
can sustain transmission of the new influenza A(H1N1) virus among
themselves. Available data are not enough to investigate the precise
role of age-specific effects (e.g. different roles of transmission
among infants, primary-school, high-school and university students)
due to small case counts. Nevertheless, we believe that the
population of minors could play a key role as a “reservoir” for
sustained chains of secondary transmission, despite the fact that
cases in this group include those infected in some atypical school
clusters. Should further data confirm these results then the value
of public health interventions targeting minors (closing schools and
further contact restrictions between minors) could be effective in
controlling further outbreaks in Japan and other countries.
Note: Each element of the next-generation matrix, i.e., R cc , R ca , R ac and
R aa , denotes the average number of secondary transmissions caused by
a single primary case for child-to-child, adult-to-child, child-to-adult
and adult-to-adult transmissions, respectively (note that here “child”
represents “minor”, aged from 0 to 19 years). The reproduction number
R, for the whole population, is given by the largest eigenvalue of the
next-generation matrix. By making qualitative assumptions A and B, two
parameters, a and b, are estimated.
4
Our estimates of Rt provide a quantitative measure of the timeevolution of the “force” of the epidemic. Although the dates of
onset have yet to be refined and, thus, the precision of Rt estimate
may have been influenced by possible delay in diagnosis and
reporting, Rt declined below 1 one day after the news of the first
three confirmed diagnoses. Thereafter, the implementation of active
surveillance programmes, including contact tracing, combined with
school closures, most likely have contributed to keeping Rt below 1.
R is useful for assessing transmission potential, and it is one of
the ways of assessing pandemic potential. This study puts emphasis
on quantifying the impact of contact patterns on the transmission
potential, factors that vary across space and time. Thus, further
analyses of R for the new influenza A(H1N1) virus in different
settings are needed to better quantify the role of uncertainty
and heterogeneous patterns of transmission in these estimates.
Validation of our quantitative understanding of the role of agespecific transmission should lead to improved effectiveness of
age-specific control measures.
Acknowledgem ents
The work of H Nishiura was partly supported by The Netherlands
Organization for Scientific Research (NWO; grant ID: 851.40.074).
References
1. Coulombier D, Giesecke J. Why are Mexican data important?. Euro Surveill.
2009;14(19):pii=19212. Available from: http://www.eurosurveillance.org/
ViewArticle.aspx?ArticleId=19212
2. Fraser C, Donnelly CA, Cauchemez S, Hanage WP, van Kerkhove MD, Hollingsworth
TD, et al. Pandemic potential of a strain of influenza A (H1N1): early findings.
Published 11 May 2009 on Science Express. Doi: 10.1126/science.1176062.
Available from: http://www.sciencemag.org/cgi/content/abstract/1176062
3. Boëlle PY, Bernillon P, Desenclos JC. A preliminary estimation of the
reproduction ratio for new influenza A(H1N1) from the outbreak in Mexico,
March-April 2009. Euro Surveill. 2009; 14(19): p11=19205. Available from: http://
www.eurosurveillance.org/ViewArticle.aspx?ArticleId=19205
5. Andreasen V, Viboud C, Simonsen L. Epidemiologic characterization of the 1918
influenza pandemic summer wave in Copenhagen: implications for pandemic
control strategies. J Infect Dis. 2008;197(2):270-8.
6. Ministry of Health, Labor and Welfare, Japan. Influenza A(H1N1). Tokyo: Ministry
of Health, Labor and Welfare; 1 June 2009. Available from: http://www.mhlw.
go.jp/english/topics/influenza_a/index.html
7.
Surveillance Group for New Influenza A(H1N1) Virus Investigation and Control
in Spain. New influenza A(H1N1) virus infections in Spain, April-May 2009. Euro
Surveill . 2009; 14(19): p11=19209. Available from: http://www.eurosurveillance.
org/ViewArticle.aspx?ArticleId=19209
8. National Institute of Infectious Diseases, Kobe Institute of Health. Interim
report on clinical presentation of the novel influenza A(H1N1) cases reported
from Kobe City. Tokyo: National Institute of Infectious Diseases; 19 May 2009.
Available from: http://idsc.nih.go.jp/disease/swine_influenza_e/idsc_e2009/
clinical_epi_kobe.html
9. Bailey NTJ. The elements of stochastic processes with applications to the
natural sciences. New York: Wiley; 1964.
10. Roberts MG, Heesterbeek JA. Model-consistent estimation of the basic
reproduction number from the incidence of an emerging infection. J Math
Biol. 2007;55(5-6):803-16.
11. Nishiura H, Chowell G, Heesterbeek H, Wallinga J. The ideal reporting interval
for an epidemic to objectively interpret the epidemiological time course. J
R Soc Interface. 2009. [In press]
12. Nishiura H, Hoye B, Klaassen M, Bauer S, Heesterbeek H. How to find natural
reservoir hosts from endemic prevalence in a multi-host population. A case
study of influenza in waterfowl. Epidemics. 2009. [In press] (Doi: 10.1016/j.
epidem.2009.04.002).
13. Chowell G, Miller MA, Viboud C. Seasonal influenza in the United States,
France, and Australia: transmission and prospects for control. Epidemiol
Infect. 2008;136(6):852-64.
This article was published on 4 June 2009.
Citation style for this article: Nishiura H, Castillo-Chavez C, Safan M, Chowell G.
Transmission potential of the new influenza A(H1N1) virus and its age-specificity
in Japan. Euro Surveill. 2009;14(22):pii=19227. Available online: http://www.
eurosurveillance.org/ViewArticle.aspx?ArticleId=19227
4. Mills CE, Robins JM, Lipsitch M. Transmissibility of 1918 pandemic influenza.
Nature. 2004; 432(7019):904-6.
Figure 4
Estimates of the reproduction number for the epidemic of new influenza A(H1N1) virus infection in Japan
A) Estimated reproduction number R, based on the initial growth phase of the epidemic (i.e. first eight days)
B) Effective reproduction number Rt , as a function of time
A
B
6
9.0
8.0
Effective reproduction number
Reproduction number
5
4
3
2
1
Mean generation time (days)
7.0
2.5
6.0
1.9
5.0
1.3
4.0
3.0
2.0
1.0
0
3.4
3.7
4.0
23-May
3.1
21-May
2.8
19-May
2.5
17-May
2.2
15-May
1.9
13-May
1.6
11-May
1.3
9-May
0.0
1.0
Mean generation time (days)
Note:
A) Mean and variance of the generation time were 1.9 days and 0.8 days2 (given a coefficient of variation of 47%), and the sensitivity of R to different
mean generation times is examined. Coefficient of variation is kept constant when the mean generation time is varied.
B) R t > 1 indicates growth of cases at a given point of time, while R t < 1 indicates that the epidemic is in declining trend and may be under control. The
horizontal dashed line represents the threshold value, R t = 1. It should be noted that the dates of onset in Japan have yet to be refined, and the precision
of R t estimate may have been influenced by possible delay in diagnosis and reporting
Epi de m iology of n ew i n flu e nza A (H1N1) vi rus
infection, United Kingdom, April – June 2009
Health Protection Agency, Health Protection Scotland, National Public Health Service for Wales, HPA Northern Ireland
Swine influenza investigation teams ([email protected])1,2,3,4
1.Health Protection Agency, London, United Kingdom
2.Health Protection Scotland, Glasgow, United Kingdom
3.National Public Health Service for Wales, Cardiff, United Kingdom
4.HPA Northern Ireland, Belfast, United Kingdom
Following the previous report to Eurosurveillance on 14 May
2009, the number of confirmed cases of new influenza A(H1N1)
has continued to increase in the United Kingdom. By 31 May,
UK surveillance activities had detected a total of 252 confirmed
cases. Seventy (28%) were related to travel to the United States
and Mexico. There is evidence of spread in households, schools
and the community with increases in secondary (n=40), tertiary
(n=125) and sporadic (n=13) cases. The new influenza A(H1N1)
virus infection continues to cause a mild illness predominately
affecting younger age-groups with a low rate of hospitalisation.
During the period from 27 April to 31 May, a total of 252
confirmed cases have been detected (Figure 1). Initially cases
were reported amongst travellers returning from Mexico, and then
from the United States. The first indigenously acquired infections
in the UK were reported on 1 May and since then the proportion
and number of indigenously acquired cases has steadily increased.
Since the identification in late April of cases of acute respiratory
infection due to a new influenza A (H1N1) virus in the United
States and Mexico [1], the same strain has been detected in an
increasing number of countries. By 31 May, the World Health
Organization (WHO) had reported 15,510 cases in 53 countries.
Of the 252 cases, 28 reported a history of travel in the seven
days before disease onset to Mexico and 42 to the United States.
Of the remaining 182, 178 cases reported no recent overseas travel
and acquired their infection within the United Kingdom. Of these
The first two confirmed cases of new influenza A(H1N1) virus
infection in the United Kingdom (UK) were reported in travellers
returning from Mexico to Scotland. The UK response and preliminary
epidemiological findings have previously been described [2]. This
article provides an update to that report.
Figure 2
Of the 252 confirmed cases, 118 (47%) are female (Figure 2).
Cases range in age from 0 to 73 years, with a mean age of 20 years
and median age of 12 years.
Cases of laboratory confirmed new influenza A(H1N1) by
age-group and sex, United Kingdom, 31 May 2009 (n=251*)
60
Figure 1
Number of confirmed cases
140
Imported
Indigenous sporadic
Indigenous tertiary
Not clear
Secondary (import related)
120
100
Number of Cases
50
Cumulative number of laboratory-confirmed new influenza
A(H1N1) cases by day of report and travel history, United
Kingdom, 31 May 2009 (n=252)
40
Female
Male
30
20
80
60
10
40
20
0
0-9
10-19
20-29
31/05
29/05
27/05
25/05
23/05
21/05
19/05
17/05
15/05
13/05
11/05
09/05
07/05
05/05
03/05
01/05
29/04
27/04
Date
6
30-39
40-49
Age-group
0
*Age missing for one case.
50-59
60-69
70-79
178 indigenous cases, 40 were secondary (contact within seven
days of onset with a travel-associated case); 125 were tertiary
Figure 3
Setting/source of acquisition of new influenza A(H1N1) virus
infection, United Kingdom, 31 May 2009 (n=238*)
Healthcare
Workplace
The First Few Hundred (FF100) project aims to collect information
about a limited number of the earliest laboratory-confirmed cases
of new influenza A(H1N1) and their close contacts [3] to gain an
early understanding of some of the key clinical, epidemiological,
and virological parameters of this infection and to facilitate real
time modelling efforts. By 31 May, 175 confirmed cases had been
entered into the FF-100 database. Clinical information gathered on
these cases shows they continue to present with symptoms typical
for influenza (Figure 4).
1
2
Other
9
Community
13
Household
42
Outside UK
70
School
101
0
20
40
60
80
100
(contact within seven days of onset with a secondary case) and
13 sporadic (no travel or contact with a confirmed case in the
seven days before onset). Follow-up is still underway for four cases.
Amongst the indigenous cases, infection has been linked to likely
transmission in a school setting for 101 cases, a household setting
for 42 cases, workplace for two cases and health care setting for
one case (Figure 3).
120
Up to 31 May, four cases have been hospitalised for clinical
reasons. No UK case is known to have died.
Number of cases
* Investigation is still underway for 14 cases.
Figure 4
Clinical presentation of confirmed cases of new influenza A(H1N1) virus infection, United Kingdom, 31 May 2009 (n=175)
Seizures
Altered consciousness
Rash
Epistaxis
Conjunctivitis
Shortness of Breath
Diarrhoea
Vomiting
Productive cough
Nausea
Arthralgia
Sneezing
Myalgia
Anorexia
Chills
Coryza
Dry cough
Headache
Malaise
Sore Throat
Fever
0%
10%
20%
30%
40%
50%
60%
70%
80%
90%
E U RO S U R V E I L L A N C E Vol . 14 · I ssu e 22 · 4 J u n e 20 0 9 · w w w. e u ros u rve ill an c e . o rg 100%
7
HPA and the Health Protection organisations for Scotland,
Wales and Northern Ireland have a number of enhanced influenza
surveillance systems that are currently operational [4] and that
provide an indication of influenza activity in the general population:
• A number of general practitioner (GP) sentinel schemes that
collect information on patient consultation rates with influenzalike illness;
• National Health Service (NHS) direct and NHS-24 telephony
systems which monitor call rates for colds/flu in the community;
• GP sentinel virological surveillance schemes to monitor
circulating respiratory viruses in the community;
• Mortality surveillance based on routine death registration data.
To date, there have not been significant signals of increased
influenza activity through these systems, which have established
thresholds for widespread circulation of influenza. Outputs from
these systems are published on a daily and weekly basis on the
HPA website [5]. Further work is on-going to describe more fully the
emerging epidemiological, virological and clinical characteristics
of this novel influenza virus including in-depth field investigations
of individual cluster events in settings such as schools.
References
1. Centers for Disease Control and Prevention (CDC). Swine influenza A (H1N1)
infection in two children – Southern California, March-April 2009. MMWR Morb
Mortal Wkly Rep. 2009;58(15):400-2.
2. Health Protection Agency and Health Protection Scotland new influenza A(H1N1)
investigation teams. Epidemiolog y of new influenza A(H1N1) in the United
Kingdom, April – May 2009. Euro Surveill. 2009;14(19):pii=19213. Available
from: http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=19213
3. McMenamin J, Phin N, Smyth B, Couzens Z, Nguyen-Van-Tam JS. Minimum dataset
for confirmed human cases of influenza H5N1. Lancet. 2008;372(9640):696-7.
4. Health Protection Agency (HPA). HPA Surveillance Systems: Swine
Influenza (H1N1swl). Available from: http://www.hpa.org.uk/webw/
HPAweb&Page&HPAwebAutoListName/Page/1243928258590?p=1243928258590
5. Health Protection Agency (HPA). HPA daily and weekly influenza report.
Available from: http://www.hpa.org.uk/webw/HPAweb&HPAwebStandard/Page/
1242949541993?p=1242949541993
Citation style for this article: Health Protection Agency, Health Protection Scotland,
National Public Health Service for Wales, HPA Northern Ireland Swine influenza
investigation teams. Epidemiology of new influenza A (H1N1) virus infection, United
Kingdom, April – June 2009. Euro Surveill. 2009;14(22):pii=19232. Available online:
http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=19232
8
E va l u at i o n
o f f o u r r e a l - t i m e PCR a s s ay s f o r
detection of influenza A(H1N1)v viruses
J Ellis ( [email protected])1, M Iturriza1, R Allan1 *, A Bermingham1, K Brown1, J Gray1, D Brown1
1.Virus Reference Department, Centre for Infections, Health Protection Agency, Colindale, London, United Kingdom
The sensitivity and specificity of four real-time PCR assays (HPA
A(H1)v, CDC A (H1)v, HPA A(N1)v and NVRL S-OIV assays) were
evaluated for detection of influenza A(H1N1)v viruses. Nose and
throat swab samples containing influenza A(H1N1)v viruses,
seasonal influenza AH3N2, AH1N1, influenza B viruses, or negative
for influenza viruses were tested by the four assays. Specificity was
also analysed using influenza A viruses of different subtypes and
non-related respiratory viruses. The sensitivities and specificities of
the four assays were in a similar range and suitable for diagnostic
use. The HPA (H1)v and the S-OIV assays were the most sensitive
assays for use as a first line test, but the S-OIV assay was less
specific, detecting all avian subtypes of influenza A viruses tested.
The results of this study demonstrate that the concurrent use of
primary diagnostic and confirmatory assays provides rapid and
accurate assessment of confirmed cases, and allows appropriate
management of patients.
Introduction
The recent emergence of new influenza A(H1N1) virus
(henceforth: influenza A(H1N1)v virus, where v stands for variant,
according to nomenclature agreed by the World Health Organization
Global Influenza Surveillance Network – WHO GISN) in humans
[1-2] has led to the requirement for sensitive and specific assays for
the differential diagnosis and confirmation of influenza A(H1N1)v
virus infections, necessary to guide public health actions. Real-time
PCR is widely considered the gold standard for molecular detection
of influenza viruses due to its high assay specificity, sensitivity and
broad linear dynamic range. In the present study, the performance
(including sensitivity and specificity) of four real-time PCR assays
designed to detect influenza A(H1N1)v viruses in respiratory
specimens has been evaluated. Two assays are based on detection
of haemagglutinin (HA), one on the detection of neuraminidase
(NA) and one on the matrix (M) gene.
HPA (H1)v assay
The influenza A(H1)v specific assay of the Health Protection
Agency (HPA) contains primers and a dual-labelled TaqMan MGB
probe (Applied Biosystems) targeting conserved sequences in
the HA gene of A(H1N1)v viruses, and the positive control swine
A(H1N1) virus A/Aragon/3218/2009, in a 1-step TaqMan PCR
assay [3]. The advantage of using a genetically distinct positive
control virus (A/Aragon/3218/2008) is that false positives can be
differentiated by sequence from true positives.
CDC (H1)v assay
The Centers for Disease Control and Prevention (CDC) realtime RT-PCR kit designed for the detection and characterisation
of influenza A(H1N1)v viruses contains a panel of oligonucleotide
primers and dual-labelled hydrolysis probes [4]. The CDC (H1)v
primer and probe set evaluated in this study has been designed to
specifically detect A(H1)v influenza in a one-step RT-PCR assay.
HPA (N1)v assay
The influenza A(N1)v real-time assay (HPA) is a two-step
TaqMan PCR assay incorporating oligonucleotide primers and
a dual-labelled MGB TaqMan probe for the detection of the NA
gene of influenza A(H1N1)v viruses and the positive control virus
A/Aragon/3218/2008 [5]. The assay has been designed to be
performed in conjunction with the influenza A(H1)v specific assay,
to provide confirmation of diagnosis of influenza A(H1N1)v virus
infection.
S-OIV assay
The swine-origin influenza virus (S-OIV) assay (National Virus
Reference Laboratory, NVRL, Dublin) is a real-time one-step RTPCR assay containing primers and a dual-labelled hydrolysis probe
targeting the M gene of influenza A viruses other than seasonal
A(H1N1) and A(H3N2) viruses [6].
Methods
Respiratory samples (85 nose or throat swabs) were submitted
as part of the influenza A(H1N1)v virus investigation in the United
Kingdom. Of these, 43 influenza A-positive, untypable, M gene
sequence-confirmed cases of influenza A(H1N1)v, and 42 A(H1N1)
v-negative samples containing seasonal influenza A(H1N1),
A(H3N2) or influenza B, or negative for influenza viruses, were
analysed using the real-time assays. In addition, specificity was
evaluated using representative influenza A viruses of HA subtype
H5, H6, H7 and H9, and a panel of non-related respiratory viruses:
respiratory syncytial viruses (RSV A and RSV B), parainfluenza
viruses, rhinoviruses, human metapneumoviruses (hMPV) and
corona viruses. Viral RNA was purified from clinical samples and
viral cultures using the Biomerieux NucliSens easyMAG system.
Specimens were tested according to the protocol provided for
each assay. All assays were run on an ABI Taqman 7500 Fast
Thermal Cycler in standard (one-step assays) or Fast (two-step)
mode. All samples were tested in duplicate. Discrepant results were
confirmed by repeat testing. Ct values of <40.00 were considered
to be positive for detection of viral RNA.
Results
The relative sensitivity of the assays was compared by analysing
a 10-fold dilution series of A/England/195/2009(H1N1)v (nose
swab sample).
No cross-reaction was observed when the four real-time assays
were used to test 22 seasonal influenza viruses, or other respiratory
viruses. A panel of representative influenza A viruses of different
subtypes was also analysed (Table 2).
The HPA (H1)v and CDC (H1)v specific assays showed no crossreactivity with any of the other influenza A subtypes analysed. The
HPA (N1)v confirmatory assay detected one influenza A(H5N1)
virus, but showed no cross-reactivity with other subtype viruses.
The S-OIV assay showed cross-reactivity with all of the influenza
A viruses analysed.
When 43 true positive samples were analysed, 36 were positive
in all four real-time PCR assays (Table 3).
Four false negative and two equivocal results were observed
with the CDC (H1)v assay. One equivocal result was observed with
the S-OIV assay. Two samples were negative with either the HPA
(H1)v or (N1)v assays, but when these assays were performed in
parallel, as recommended, one false negative result was observed.
No false-positives were detected in the 42 influenza A(H1N1)v
virus-negative samples with any of the four real-time assays.
The Ct values obtained by analyses with the real-time assays of
the 43 confirmed influenza A (H1N1)v virus samples are shown
in Figures 1a-c. A total of 42 true negative and 43 true positive
samples were tested in all assays. Comparison of the HPA (H1)v and
CDC (H1)v assays showed that of the 43 true positives tested, 41
were detected in the HPA (H1)v assay (Figure 1a). Thirty seven were
positive and 2 equivocal in the CDC (H1)v assay. Three samples
positive in HPA (H1)v assay were negative in the CDC assay and 1
sample positive in the HPA (H1)v assay was equivocal in the CDC
(H1)v assay.
Of the 43 true positives, 41 were positive in the HPA (H1)v
assay and 42 in the S-OIV assay (Figure 1b). One sample gave an
equivocal result with the S-OIV assay.
Comparison of the HPA (H1)v diagnostic assay with the HPA
(N1)v confirmatory assay demonstrated that the two assays correlate
well, with a correlation coefficient of r = 0.97 (Figure 1c).
The precision of the HPA (H1)v and (N1)v real-time assays was
assessed by the coefficient of variation (CV) and standard deviation
(SD) of the replicate Ct measurements (n=37 and n=9 respectively)
for the assay-positive control on diagnostic assay runs. The CV
for the mean Ct values obtained with the (H1)v and (N1)v assaypositive controls was 3% and 2% respectively.
Ta b l e 1
End-point detection of A/England/195/2009 (H1N1)v by four real-time PCR assays
Mean Ct values
Dilution A/Eng/195/2009(H1N1)v
HPA (H1)v
CDC (H1)v
HPA
(N1)v
S-OIV
1.00E-03
18.35
24.85
23.50
21.85
1.00E-04
21.35
28.25
27.15
25.30
1.00E-05
24.60
31.75
30.60
28.45
1.00E-06
27.95
35.20
34.25
31.70
1.00E-07
30.65
38.70
36.10
37.60
1.00E-08
32.95
Neg
38.80
36.85
1.00E-09
Neg
Neg
Neg
Neg
Ta b l e 2
Specificity of four real-time PCR assays with representative influenza A subtype virus isolates
Influenza A virus subtype
a
HPA (H1)v
CDC (H1)v
HPA (N1)v
S-OIV
A/Cambodia/R0405050/2007 RGa H5N1
Neg
Neg
Neg
28.02
A/Indonesia/6/2005 H5N1
Neg
Neg
31.77
27.27
A/Chicken/Turkiye/Av05/2006 H5N1
Neg
Neg
Neg
25.92
A/Vietnam/1203/2004 H5N1
Neg
Neg
Neg
27.36
A/Duck/Singapore-Q/F119-3/97 H5N3
Neg
Neg
Neg
22.53
A Turkey/England/198/2009 H6N1
Neg
Neg
Neg
30.61
A/AfricanStarling/Q-England/983/79 H7N1
Neg
Neg
Neg
29.06
A/Chicken/Wales/306/2007 H7N2
Neg
Neg
Neg
30.54
A/Quail/HongKong/G1/97 H9N2
Neg
Neg
not done
26.08
derived by reverse genetics
10
Ta b l e 3
Comparison of HPA (H1)v, CDC (H1)v, HPA (N1)v, and S-OIV
real-time PCR assays on sequence confirmed swine-lineage samples
Number of samples
HPA (H1)v
CDC (H1)v
HPA (N1)v
36
+
+
+
+
1
+
-
+
Equiv*
2
+
-
+
+
1
-
+
+
+
1
-
-
-
+
1
+
Equiv*
+
+
1
+
Equiv*
-
+
95.4
90.7
95.4
100
Sensitivity (%)
S-OIV
Because the security of a diagnostic result for influenza A(H1N1)
v virus is important for public health actions, the use of primary
detection and confirmatory assays as described here is appropriate.
The use of the HPA (H1)v and (N1)v assays together provides
rapid and accurate assessment of confirmed cases, and enables
appropriate management of patients.
* Weak positive in one replicate
Figure 1a
Comparison of HPA (H1)v and CDC (H1)v assay Ct values
A ck now led gem e nts
The authors would like to acknowledge the contribution of the
member laboratories of the Regional Microbiolog y Network, HPA,
and participating Royal College of General Practitioners practices,
in submitting the clinical samples evaluated in this study. The S-OIV
real-time PCR assay protocol and primer and probe sequences were
kindly provided by M Carr and S Coughlan (NVRL, Dublin). The influenza
A(H1N1) virus A/Aragon/3218/2008 was kindly provided by the Director
of the National Centre for Microbiolog y, Instituto de Salud Carlos III,
Madrid, Spain. Technical assistance in performing the evaluation was
provided by T Talts and C Amar.
HPA (H1)v vs CDC (H1)v assay
45
y 2= 1.0717x - 3.2748
R = 0.8959
CDC (H1)v
40
35
30
25
20
15
15
20
25
30
35
40
45
HPA (H1)v
References
1. Novel Swine-Origin Influenza A (H1N1) Virus Investigation Team. Emergence
of a Novel Swine-Origin Influenza A (H1N1) Virus in Humans. N Engl J Med.
22 May 2009. [Epub ahead of print].
Figure 1b
Comparison HPA (H1)v and S-OIV assay Ct values
40
3. Health Protection Agency (HPA). Swine-Lineage Influenza A H1 Specific Fast
Real Time PCR. National Standard Methods - Virology. VSOP 29, Issue 2, May
2009. Available from: http://www.hpa-standardmethods.org.uk/pdf_sops.asp
y = 1.0233x - 1.4958
R2 = 0.9335
35
S-OIV
2. Centers for Disease Control and Prevention (CDC). Swine influenza A (H1N1)
infection in two children – Southern California, March-April 2009. MMWR Morb
Mortal Wkly Rep 2009;58(15):400-2
HPA (H1)v vs S-OIV
45
4. World Health Organization (WHO). CDC protocol of realtime RTPCR for influenza
A (H1N1). 30 April 2009. Available from: http://www.who.int/csr/resources/
publications/swineflu/realtimeptpcr/en/index.html
30
25
20
15
15
20
25
Conclusions
The sensitivities and specificities of the four assays were in a
similar range and suitable for diagnostic use. The HPA (H1)v and
the S-OIV assays were the most sensitive assays for use as a first
line test, but the S-OIV assay was less specific, detecting all avian
subtypes of influenza A viruses tested. For confirmation, an assay in
another gene such as the HPA (N1)v could be employed. The results
obtained with the HPA (H1)v and (N1)v assays correlated well and,
in addition, intra-assay variability of the HPA (H1)v and (N1)v
assays was shown to be acceptable with values for the coefficient
of variation (CV) <5%.
30
35
40
45
HPA (H1)v
5. Health Protection Agency (HPA). Swine-lineage Influenza A N1 Fast Real Time
Confirmatory PCR assay. National Standard Methods – Virology. VSOP 48, Issue
1, May 2009. Available from: http://www.hpa-standardmethods.org.uk/pdf_sops.
asp
6. Personal communication from Dr Michael Carr, National Virus Reference
Laboratory (NVRL), Dublin, 22 May 2009.
Figure 1c
Correlation of Ct values obtained with HPA (H1)v and (N1)
v assays
Correlation of HPA (H1)v vs (N1)v assays
45
y 2= 0.8842x + 4.6482
R = 0.9449
HPA (N1)v
40
Citation style for this article: Ellis J, Iturriza M, Allen R, Bermingham A, Brown K,
Gray J, Brown D. Evaluation of four real-time PCR assays for detection of influenza
A(H1N1)v viruses. Euro Surveill. 2009;14(22):pii=19230. Available online: http://www.
*Authors’ correction:
The name of the third author was corrected on 13 June 2012 at the request of the
authors.
35
30
25
20
15
15
20
25
30
35
40
45
HPA (H1)v
Origins
of the new influenza
ta k e a c t i o n
A(H1N1)
v i r u s : t i m e to
G M Nava ([email protected])1,2, M S Attene-Ramos2, J K Ang2, M Escorcia1
1.Facultad de Medicina Veterinaria y Zootecnia (College of Veterinary Medicine), Universidad Nacional Autonoma de Mexico
(National Autonomous University of Mexico), Mexico City, Mexico
2.Institute for Genomic Biolog y, University of Illinois at Urbana-Champaign, United States
To gain insight into the possible origins of the 2009 outbreak of
new influenza A(H1N1), we performed two independent analyses
of genetic evolution of the new influenza A(H1N1) virus. Firstly,
protein homology analyses of more than 400 sequences revealed
that this virus most likely evolved from recent swine viruses.
Secondly, phylogenetic analyses of 5,214 protein sequences of
influenza A(H1N1) viruses (avian, swine and human) circulating
in North America for the last two decades (from 1989 to 2009)
indicated that the new influenza A(H1N1) virus possesses a
distinctive evolutionary trait (genetic distinctness). This appears
to be a particular characteristic in pig-human interspecies
transmission of influenza A. Thus these analyses contribute to
the evidence of the role of pig populations as “mixing vessels” for
influenza A(H1N1) viruses.
Introduction
On 24 April, the World Health Organization (WHO) released
the first alert indicating the occurrence of confirmed human cases
of swine influenza A(H1N1) in North America [1]. A few days
later, the Centers for Disease Control and Prevention in the United
States confirmed that these human influenza cases were caused
by the same new influenza A(H1N1) virus [2]. Soon after, it was
proposed that the current flu outbreak is caused by a new influenza
A(H1N1) virus generated from a triple reassortment of human,
swine and avian viruses [2-8]. Other publications, including our
study presented here, demonstrate that this new influenza A(H1N1)
virus most likely evolved from recent swine viruses [9-11].
Methods and results
Protein homology analysis
We used more than 400 protein sequences to analyse the genetic
evolution of the new influenza A(H1N1) virus. This set of protein
sequences included polymerases PB2, PB1 and PA, hemagglutinin
(HA), nucleocapsid (NP), neuraminidase (NA), matrix 1 (MP1),
nonstructural 1 (NS1) encoded by the new influenza A(H1N1) virus
as well as other homologous proteins from influenza viruses from
past flu seasons. Phylogenetic tree topologies revealed that the
closest homologies for the new influenza A(H1N1) virus are swine
influenza viruses that have been circulating in the United States
and Asia for the last decade (Figure 1, Supplementary materials:
Figure 1 and Table 1).
Figure 1. Possible origins of the influenza 2009 A(H1N1) virus:
a) hemagglutinin and b) neuraminidase proteins
(See Below)
12 These findings indicate that domestic pigs in North America
may have a central role in the generation and maintenance of this
virus. This idea is also supported by the observation that protein
sequences of the new influenza A(H1N1) virus have close homology
to proteins of swine influenza viruses that infected humans in the
recent past (Supplementary materials: Figure 1, Figure 2 and Table
2). In fact, a common element of these swine influenza zoonotic
transmissions was that humans (mostly swine farm workers) were
in direct contact with infected pigs [12-15].
Phylogenetic analysis
To further examine the possible genetic origins of the new
influenza A(H1N1) virus, we compared all the available sequences
of influenza A(H1N1) viruses circulating in North America for the
last two decades (from 1989 to 2009). Protein sequences from
avian, swine and human influenza viruses were obtained from
the Influenza Virus Resource [16], a database that integrates
information gathered from the Influenza Genome Sequencing
Project of the National Institute of Allergy and Infectious Diseases
(NIAID) and the GenBank of the National Center for Biotechnology
Information (NCBI). A total of 5,214 protein sequences were found
in this database. After removing identical sequences, a set of 1,699
influenza A proteins including PB2, PB1, PA, HA, NP, NA, MP1,
and NS1 proteins were used for analyses of the genetic evolution
of influenza A(H1N1) viruses. These analyses provide additional
evidence of the role of pig populations as “mixing vessels” for
influenza A(H1N1) viruses (Figure 2).
Figure 2. Genetic distinctness of the influenza 2009 A(H1N1)
virus: a) hemagglutinin (HA) and b) neuraminidase (NA) proteins;
c) phylogenetic trees for PB2, PB1, PA, NP, MP1, and NS1 proteins
(See Below)
Secondly, our analyses also revealed that the new influenza
A(H1N1) virus possesses a distinctive evolutionary trait (genetic
distinctness), that seems to be characteristic in pig-human
interspecies transmission of influenza A (reported cases occurred
in Iowa, Maryland and Wisconsin, United States between 1991 and
2006) (Figure 2, Supplementary materials: Figure 2 and Table 3).
Discussion and conclusion
Although limited in sample size, our analyses substantiate
the value of molecular screening and phylogenetic assessment
for understanding the evolution of influenza viruses and, most
importantly, for the early detection of emerging novel viruses that
could lead to influenza pandemics. Notably, our analyses revealed
that the new influenza A(H1N1) virus is genetically distinct from
other influenza A(H1N1) viruses that have been circulating for the
last twenty flu seasons (Figure 2 and Supplementary materials:
Figure 2). Influenza viruses with novel antigens (genetic drift)
can escape from immune responses induced by prior infection or
vaccination and can lead to a pandemic [17].
2. Centers for Disease Control and Prevention (CDC). Update: swine influenza
A(H1N1) infections – California and Texas, April 2009. MMWR Morb Mortal Wkly
Rep 2009;58(16):435-7.
These observations also reiterate the potential risk of pig
populations as the source of the next influenza virus pandemic.
Although the role of swine as “mixing vessels” for influenza
A(H1N1) viruses was established more than a decade ago [18,19],
it appears that the policy makers and scientific community have
underestimated it. In fact, in 1998 influenza experts proposed the
establishment of surveillance in swine populations as a major part
of an integrated early warning system to detect pandemic threats
for humans [18,19] but, to some extent, this task was overlooked.
For example, a search of influenza sequences in the Influenza Virus
Resource [16] revealed that the total number of swine influenza
A sequences (as of 19 May 2009) is ten-times smaller than the
corresponding number of human and avian influenza A sequences
(4,648 compared to 46,911 and 41,142 sequences, respectively).
More significantly, in some countries, such as the United States, the
national strategy for pandemic influenza [20] assigned the entire
preparedness budget (3.8 billion US dollars) for the prevention and
control of avian A(H5N1) influenza, overlooking the swine threat
[20-22]. In our (the authors’) opinion, in this plan, a substantial
effort was dedicated to prevent and contain the foreign threat of
Asian avian flu, neglecting the influenza threat that the North
American swine population presents [23]. Specifically, we believe
that the aforementioned strategy ignores the swine farm and
industry workers which constitute the population at higher risk of
contracting and spreading the hypothetical pandemic influenza
virus [24-26].
5. Anonymous. Swine influenza: how much of a global threat? Lancet.
2009;373(9674):1495.
The current new influenza A(H1N1) outbreak caused by a virus
of swine origin represents a new challenge for animal and human
health experts. Our institution, the College of Veterinary Medicine
at the National Autonomous University of Mexico (Universidad
Nacional Autonoma de Mexico, UNAM) is placing a strong emphasis
on the establishment of influenza surveillance in swine and avian
species to identify novel genetic assortment of the new influenza
A(H1N1) and other influenza viruses circulating in Mexico. For
example, since 2002, we have been monitoring the genetic
evolution of influenza A viruses circulating in Mexican poultry
farms [27]. Now, a similar surveillance system will be applied to
swine farms. This effort prioritises the use of genetic distinctness
as a marker for the detection of novel viruses that could lead to
influenza pandemics.
17. Hilleman MR. Realities and enigmas of human viral influenza: pathogenesis,
epidemiology and control. Vaccine 2002;20(25-26):3068-87.
The recent influenza pandemic threat in North America reveals
that it is time to take action towards the development of a systemic
surveillance system which integrates phylogenetic information of
influenza viruses circulating in humans and livestock.
Supplementary materials: Figure 1, Figure 2, Table 1, Table
2, Table 3:
(See Below)
References
1. World Health Organization (WHO). Influenza-like illness in the United States
and Mexico. Epidemic and Pandemic Alert and Response (EPR). 24 April 2009.
Available from: http://www.who.int/csr/don/2009_04_24/en/index.html
3. Cohen J, Enserink M. Infectious diseases. As swine flu circles globe, scientists
grapple with basic questions. Science. 2009;324(5927):572-3.
4. Centers for Disease Control and Prevention (CDC). Swine influenza A(H1N1)
infection in two children – Southern California, March-April 2009. MMWR
Morb Mortal Wkly Rep 2009;58(15):400-2.
6. Cohen J. Swine flu outbreak. Out of Mexico? Scientists ponder swine flu’s
origins. Science. 2009;324(5928):700-2.
7.
Butler D. Swine flu goes global. Nature. 2009;458(7242):1082-3.
8. Cohen J. Swine flu outbreak. Flu researchers train sights on novel tricks of
novel H1N1. Science. 2009;324(5929):870-1.
9. Garten RJ, Davis CT, Russell CA, Shu B, Lindstrom S, Balish A, et al. Antigenic
and Genetic Characteristics of Swine-Origin 2009 A(H1N1) Influenza Viruses
Circulating in Humans. Science. 22 May 2009 [Epub ahead of print] DOI:
10.1126/science.1176225
10. Solovyov A, Palacios G, Briese T, Lipkin WI, Rabadan R. Cluster analysis
of the origins of the new influenza A(H1N1) virus. Euro Surveill.
2009;14(21):pii=19224. Available from: http://www.eurosurveillance.org/
ViewArticle.aspx?ArticleId=19224
11. Novel Swine-Origin Influenza A (H1N1) Virus Investigation Team. Emergence
of a Novel Swine-Origin Influenza A (H1N1) Virus in Humans. N Engl J Med.
22 May 2009. [Epub ahead of print].
12. Gray GC, McCarthy T, Capuano AW, Setterquist SF, Olsen CW, Alavanja MC.
Swine workers and swine influenza virus infections. Emerg Infect Dis.
2007;13(12):1871-8.
13. Wentworth DE, Thompson BL, Xu X, Regnery HL, Cooley AJ, McGregor MW, et
al. An influenza A (H1N1) virus, closely related to swine influenza virus,
responsible for a fatal case of human influenza. J Virol. 1994;68(4):2051-8.
14. Gregory V, Lim W, Cameron K, Bennett M, Marozin S, Klimov A, et al. Infection of
a child in Hong Kong by an influenza A H3N2 virus closely related to viruses
circulating in European pigs. J Gen Virol. 2001;82(Pt 6):1397-406.
15. Olsen CW, Karasin AI, Carman S, Li Y, Bastien N, Ojkic D, et al. Triple reassortant
H3N2 influenza A viruses, Canada, 2005. Emerg Infect Dis. 2006;12(7):1132-5.
16. Bao Y, Bolotov P, Dernovoy D, Kiryutin B, Zaslavsky L, Tatusova T, et al. The
influenza virus resource at the National Center for Biotechnology Information.
J Virol. 2008;82(2):596-601.
18. Webster RG. Influenza: an emerging disease. Emerg Infect Dis. 1998;4(3):436-41.
19. Ito T, Couceiro JN, Kelm S, Baum LG, Krauss S, Castrucci MR, et al. Molecular
basis for the generation in pigs of influenza A viruses with pandemic
potential. J Virol. 1998 Sep;72(9):7367-73.
20. Homeland Security Council. National Strateg y for Pandemic Influenza.
President of the United States: Washington; November 2005. Available from:
http://www.pandemicflu.gov/plan/federal/pandemic-influenza.pdf
21. Comments from the Center for Biosecurity of UPMC on the National Strategy for
Pandemic Influenza: Implementation Plan. Biosecur Bioterror. 2006;4(3):320-4.
22. Mair M. National strateg y for pandemic influenza released; $3.8 billion
appropriated for pandemic preparedness. Biosecur Bioterror 2006;4(1):2-5.
23. Staff of the Center for Biosecurity of UPMC. National strateg y for Pandemic
Influenza and the HHS Pandemic Influenza Plan: thoughts and comments.
Biosecur Bioterror 2005;3(4):292-4.
24. Gray GC, Kayali G. Facing pandemic influenza threats: the importance of
including poultry and swine workers in preparedness plans. Poult Sci
2009;88(4):880-4.
25. Ramirez A, Capuano AW, Wellman DA, Lesher KA, Setterquist SF, Gray GC.
Preventing zoonotic influenza virus infection. Emerg Infect Dis. 2006;12(6):9961000.
26. Myers KP, Olsen CW, Setterquist SF, Capuano AW, Donham KJ, Thacker EL, et al.
Are swine workers in the United States at increased risk of infection with
zoonotic influenza virus? Clin Infect Dis. 2006;42(1):14-20.
27. Escorcia M, Vázquez L, Méndez ST, Rodríguez-Ropón A, Lucio E, Nava GM. Avian
influenza: genetic evolution under vaccination pressure. Virol J. 2008;5:15.
Citation style for this article: Nava GM, Attene-Ramos MS, Ang JK, Escorcia M. Origins of
the new influenza A(H1N1) virus: time to take action. Euro Surveill. 2009;14(22):pii=19228.
Available online: http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=19228
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a Protein sequences from the 2009 A(H1N1) virus were retrieved and used for BLAST searches versus the all-species NCBInr protein database. Top-fifty best hits were retrieved from
GenBank and used for phylogenetic tree reconstruction using the maximum parsimony method. Phylogenetic trees were rooted using the earliest influenza virus found with the analysis.
Proteins from the 2009 A(H1N1) virus (red circles) showed close homology to proteins from swine influenza viruses circulating in Asia, Europe and US (blue circles) and swine influenza
viruses that have infected humans in recent past (red squares). Protein relationships with avian influenza virus (green circles) were more distant. Scale bar indicates the number of changes
over the whole sequence. Phylogenetic trees for PB2, PB1, PA, NP, MP1, and NS1 proteins, and details of statistical significance of branch order are provided in Supplementary Materials Figure 1.
Figure 2. Genetic distinctness of the influenza 2009 A(H1N1) virus: a) hemagglutinin (HA) and b) neuraminidase (NA)
proteins; c) phylogenetic trees for PB2, PB1, PA, NP, MP1, and NS1 proteins
a Mixing vessel
HA
b
NA
2009 A(H1N1)
Genetic distinctness
5
10
14 E U R OS U R V E I L L A N C E Vol . 14 · I ss u e 22 · 4 J u n e 20 0 9 · w w w. e u ros u rve ill an c e . o rg
S u p pl e m e n t a r y m a t e r i al s fo r
Origins
of the new influenza
ta k e a c t i o n
A(H1N1)
v i r u s : t i m e to
Supplementary Fig. 1. Possible origins of influenza 2009 A(H1N1) virus. a, PB2; b, PB1 and
c, PA polymerases; d, hemagglutinin; e, nucleocapsid protein; f, neuraminidase; g, matrix
protein 1; h, nonstructural protein 1. Protein sequences from the 2009 A(H1N1) virus were
used for BLAST searches versus the all-species NCBInr protein database. Top fifty best hits
were retrieved from GenBank and used for phylogenetic tree reconstruction using the
maximum
i
parsimony
i
method.
h d Phylogenetic
Ph l
i trees were constructed
d with
i h the
h maximum
i
parsimony method using the MEGA software version 4.0 and rooted using the earliest
influenza virus isolates obtained with the analyses. The statistical significance of branch order
was estimated by the generation of 100 replications of bootstrap resampling of the originallyaligned amino acid sequences.
sequences Scale bar indicates the number of changes over the whole
sequence.
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21
E U RO S U R V E I L L A N C E Vol . 14 · I ssu e 22 · 4 J u n e 20 0 9 · w w w. e u ros u rve ill an c e . o rg NA
f
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h
23
Supplementary Fig. 2. Genetic distinctness of the influenza 2009 A(H1N1) virus. a, PB2; b,
PB1 and c, PA polymerases; d, hemagglutinin (HA); e, nucleocapsid protein (NP); f,
neuraminidase (NA); g, matrix protein 1 (MP1); h, nonstructural protein 1 (NS1). Protein
sequences from avian, swine and human influenza A (H1N1) viruses circulating in NorthAmerica from 1989 to 2009 were retrieved from the Influenza Virus Resource. Sequences were
usedd for
f unrootedd phylogenetic
h l
i tree construction
i
with
i h the
h maximum
i
parsimony
i
method.
h d
Proteins from the influenza 2009 A(H1N1) virus (red triangles), earlier human (red and pink
circles) swine (navy blue and purple circles) and avian (green circles) viruses are shown. Light
colors (pink, purple and green) correspond to viruses found between 1989 and 1999 and dark
colors (red,
(red navy blue and green) to viruses found between 2000 and 2009.
2009 Orange squares
represent pig-human interspecies transmission of influenza A cases occurred in Iowa,
Maryland and Wisconsin, USA between 1991 and 2006. Scale bar indicates the number of
changes over the whole sequence. Phylogenetic trees were constructed with the MEGA
software version 4.0. The statistical significance of branch order was estimated by the
generation of 100 replications of bootstrap resampling of the originally-aligned amino acid
sequences. Scale bar indicates the number of changes over the whole sequence.
24 E U R OS U R V E I L L A N C E Vol . 14 · I ss u e 22 · 4 J u n e 20 0 9 · w w w. e u ros u rve ill an ce . o rg
10
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32
18
Supplementary table 1. Closest protein homology of influenza 2009 A(H1N1) viruses
Gene
Best Hit
Identity
Lineage
PB2
A/Swine/Illinois/100085A/01 (H1N2)
98%
Swine
PB1
A/Wisconsin/10/98 (H1N1)
98%
Human
PA
A/Swine/Illinois/100084/01 (H1N2)
98%
Swine
HA
A/Swine/Indiana/P12439/00 (H1N2)
95%
Swine
NP
A/swine/Guangxi/13/2006 (H1N2)
98%
Swine
NA
A/swine/Spain/WVL6/1991 (H1N1)
94%
Swine
MP1
A/swine/Laer/IDT4126/05 (H3N2)
99%
Swine
NS1
A/SW/IN/14810-T/01 (H1N2)
94%
Swine
19
Supplementary table 2. Closest protein homology of influenza 2009 A(H1N1) viruses with
swine influenza viruses that have infected humans
Protein
Cases
Identity
Lineage
Reference
PB2
A/Iowa/CEID23/2005(H1N1)
98%
Human
[1]
PB1
98%
Human
ABG48024
PA
A/Ontario/RV1273/2005(H3N2)
97%
Human
[2]
HA
A/Wisconsin/10/98 (H1N1)
93%
Human
AAO88265
NP
A/Iowa/CEID23/2005(H1N1)
97%
Human
[1]
A/MD/12/1991(H1N1)
98%
Human
AAA51491
A/Ohio/3559/1988(H1N1)
98%
Human
ABU80404
A/Ohio/3523/1988(H1N1)
97%
Human
AAA73104
Nf
Nf
Nf
NA
Novel protein
MP1
A/Hong Kong/1774/99(H3N2)
99%
Human
[3]
NS1
/Wisconsin/10/1998(H1N1)
93%
Human
AAO88260
A/Ontario/RV1273/2005(H3N2)
94%
Human
[2]
Nf = Not found
20
34
Supplementary table 3. Reported cases of pig-human interspecies transmission of influenza A
(H1N1) occurred in Iowa, Maryland and Wisconsin, USA between 1991 and 2006. These
influenza virus subtypes possess genetic distinctness compared to main cluster of human
influenza A (H1N1) viruses
Influenza A virus subtype
Evidence linking pig-
Reference
human infection
A/Iowa/CEID23/2005 (H1N1)
Yes
[1]
Insufficient data
[4]
A/Wisconsin/4754/1994
Yes
[5]
A/Maryland/12/1991
Yes
[5]
A/MD/12/1991
Yes
[5]
A/Wisconsin/4755/1994
Yes
[5]
A/Wisconsin/87/2005
Yes
[6]
A/Iowa/01/2006
Yes
[6]
A/Wisconsin/10/1998
21
References
1.
2.
3.
4.
5.
6.
Gray GC, McCarthy T, Capuano AW, Setterquist SF, Olsen CW, Alavanja MC: Swine
workers and swine influenza virus infections. Emerg Infect Dis 2007, 13:1871-1878.
Olsen CW, Karasin AI, Carman S, Li Y, Bastien N, Ojkic D, Alves D, Charbonneau G,
Henning BM, Low DE, et al: Triple reassortant H3N2 influenza A viruses, Canada,
2005. Emerg Infect Dis 2006, 12:1132-1135.
Gregory V, Lim W, Cameron K, Bennett M, Marozin S, Klimov A, Hall H, Cox N, Hay
A, Lin YP: Infection of a child in Hong Kong by an influenza A H3N2 virus closely
related to viruses circulating in European pigs. J Gen Virol 2001, 82:1397-1406.
Zhou NN, Senne DA, Landgraf JS, Swenson SL, Erickson G, Rossow K, Liu L, Yoon K,
Krauss S, Webster RG: Genetic reassortment of avian, swine, and human influenza A
viruses in American pigs. J Virol 1999, 73:8851-8856.
Wentworth DE, Thompson BL, Xu X, Regnery HL, Cooley AJ, McGregor MW, Cox NJ,
Hinshaw VS: An influenza A (H1N1) virus, closely related to swine influenza virus,
responsible for a fatal case of human influenza. J Virol 1994, 68:2051-2058.
Shinde V, Bridges CB, Uyeki TM, Shu B, Balish A, Xu X, Lindstrom S, Gubareva LV,
Deyde V, Garten RJ, et al: Triple-Reassortant Swine Influenza A (H1) in Humans in
the United States, 2005-2009. N Engl J Med 2009.
22
36
E U R OS U R V E I L L A N C E Vol . 14 · I ss u e 22 · 4 J u n e 20 0 9 · w w w. e u ros u rve ill an ce . o rg
Norwegians
a p p r o v e o f t h e h e a lt h a u t h o r i t i e s ’
s t r at e g y t o c o m m u n i c at e w o r s t c a s e p a n d e m i c
scenarios
G Wøien1, K I Tonsberg ([email protected])2
1.Norwegian Institute of Public Health, Oslo, Norway
2.Department of Communication, Norwegian Directorate of Health, Oslo, Norway
According to the Norwegian pandemic preparedness plans, health
authorities shall assess their communication activities before and
during an outbreak of infectious diseases. A survey was conducted
on 29 April 2009 on acceptance of communications by the national
public health authorities concerning the emerging threat from the
new influenza A(H1N1) virus. The survey was similar to other
surveys in 2005-6 about the avian flu. The results were not very
different – the overall majority of the people interviewed were not
worried and the health authorities were regarded as trustworthy.
Introduction
Norwegian media coverage (broadcast and press) of the new
influenza A(H1N1) virus outbreak in Mexico and the Unites States
rose markedly in the days following the World Health Organization’s
(WHO) alert on 24 April 2009 [1] and a substantial number of
domestic news articles were registered. Spokespersons talking at
daily news briefings on behalf of Norway’s health authorities did
not rule out the worst case scenarios laid down in the National
Pandemic Contingency Plan. Thus, the possibility of a severe
pandemic caught the headlines which warned that the number of
deaths might equal that of the Spanish flu 90 years ago. A further
focus of the media reports was on public preparedness measures
and advice to the public.
In order to evaluate the plans for a future communication
strategy and to assess the public relations work done from 24
April to 29 April, a survey was conducted on 29 April 2009 by
one of the largest public research companies in Norway, Synovate
Research. The research was done on behalf of the Norwegian health
authorities and it took place in the hours just before WHO raised
the phase of pandemic alert level from phase 4 to phase 5.
Methods and results
The survey was conducted following standard procedures by
picking phone numbers randomly from the telephone directory.
A total of 1,368 Norwegians were contacted and 506 (37%)
interviewed, weighted according to age, sex and geographical
location to make the selection representative. They were given
the following possible answers to each of the six statements
enumerated below:
• I completely agree or partially agree
• I neither agree nor disagree
• I partially disagree or totally disagree
• I don’t know / cannot answer
The following passage presents the results for each statement.
“I am not worried about catching the ‘swine flu’ now.” Eight out
of 10 Norwegians stated that they are not worried.
“I feel confident that Norwegian health authorities are well
prepared for a possible ‘swine flu’ outbreak with human-to-human
transmission in Norway.” Eight out of 10 Norwegians are confident
that the authorities are well prepared.
“Norwegian health authorities have provided good and balanced
information about the ‘swine flu’.” Seven out of 10 respondents
consider the authorities have provided good and balanced
information.
“Norwegian health authorities have exaggerated the danger
related to the ‘swine flu’.” Five out of 10 participants do not think
the authorities have exaggerated the dangers.
“Outbreaks, such as the ‘swine flu’, should be taken seriously
because one never knows when a dangerous flu pandemic will
break out.” Nine out of 10 agree that these outbreaks should be
taken seriously.
“There is too much media focus on the ‘swine flu’.” Six out of
10 Norwegians think there is too much media focus on the topic.
Conclusions
Similar surveys on the perception of the Norwegian citizens on the
communication activities of the health authorities were conducted
in 2005 and 2006 concerning the avian flu. The maximum press
coverage on this public health event was in February-March 2005
with a focus on worst case pandemic scenarios. There were 20%
more articles about bird flu registered in the domestic press during
that period than during the influenza A(H1N1) outbreak so far. The
answers were more or less in line with this year’s survey.
Our surveys are examples of what health authorities can do to
monitor the impact of their communication efforts on national
public opinion. As all opinion polls, they are a snapshot valid for
a particular context, time and space. However, at the time of the
surveys, Norwegians seemed to be open to listening to worst case
scenarios and have confidence in the authorities.
The data presented from the survey allow for further comments.
Surveys like these may be useful when planning risk communication
strategies [2]. Further research on the topic should be inspiring for
health authorities in our as well as other countries.
References
1. World Health Organization (WHO). Influenza-like illness in the United States
and Mexico. Epidemic and Pandemic Alert and Response (EPR). 24 April 2009.
Available from: http://www.who.int/csr/don/2009_04_24/en/index.html
2. The Peter M. Sandman Risk Communication Website [homepage on the
Internet]. New York P Sandmann [updated 23 May 2009; cited 4 June 2009].
Available from: www.psandman.com/
Citation style for this article: Wøien G, Tonsberg KI. Norwegians approve of the health
authorities’ strategy to communicate worst case pandemic scenarios. Euro Surveill.
2009;14(22):pii=19231. Available online: http://www.eurosurveillance.org/ViewArticle.
aspx?ArticleId=19231
38
R e s e a r c h a r ti c l e s
A u to c h t h o n o u s
c y s t i c e c h i n o c o c c o s i s i n p at i e n t s
who grew up in Germany
J Richter ([email protected])1, A Orhun1, B Grüner2, I Müller-Stöver1, S Reuter1, T Romig3, D
Häussinger1, P Kern2
1.Tropical Medicine Unit, University Hospital for Gastroenterology, Hepatology and Infectious Diseases, Heinrich-HeineUniversity, Düsseldorf, Germany
2.Comprehensive Infectious Diseases Center (CIDC), Division of Infectious Diseases and Clinical Immunology, University
Hospital of Ulm, Germany
3.Department of Parasitolog y, University Hohenheim, Stuttgart, Germany
Human cystic echinococcosis (CE) is a widespread zoonosis. Cases
occurring in Germany are considered to result from imported
infection and it is unclear if Echinococcus granulosus (sensu lato) is
still transmitted in Germany. Therefore, exposure was investigated
in 15 patients with cystic echinococcosis (7 female, 8 male; agerange 16-68, with a median of 48 years) who grew up in Germany.
Fourteen patients had most likely acquired their infection in rural
Germany, 11 from local dogs, one from an imported dog, two without
obvious dog contacts. Taking into account multiple conceivable
confounding factors might also account for some of infections:
contacts with imported dogs or contact with dogs during travel
in highly endemic regions, and ingestion of food contaminated
by worm ova, whether in Germany or abroad. However, in at least
two cases autochthonous transmission is beyond doubt, because
these patients had never left Germany. The long pre-symptomatic
development of cystic echinococcosis does not allow for a precise
evaluation of the actual epidemiological situation. Compulsory
notification of human cystic echinococcosis is an important
instrument in the surveillance of the disease in humans. Regular
inquiries at laboratories carrying out work in the field of veterinary
medicine and at slaughterhouses, supervision of dogs at risk as
well as genetic investigations on the strain or species of the causal
agent of cystic echinococcosis are needed.
Introduction
Echinococcosis is a zoonosis occurring worldwide. Two
forms of echinococcosis can affect humans: alveolar and cystic
echinococcosis. The causal agent of alveolar echinococcosis is
Echinococcus multilocularis. It is found in foxes, dogs, cats and
wolves. The main host, the fox, contracts E. multilocularis mostly
from eating rodents. E. multilocularis is known to sporadically
transmit to humans in Germany [1, 2]. The domestic dog is the
most frequent main host for E. granulosus and life cycles occur
between dogs and different domestic animals including sheep or
pigs. Worldwide human cystic echinococcosis following infection
with several forms of the heterogeneous E. granulosus complex,
accounts for most cases of human echinococcosis. The worldwide
incidence of cystic echinococcosis is estimated to amount to
100,000 to 300,000 cases annually [3, 4]. Pastoral populations
in East Africa, Kazakhstan, Kyrgizstan, northwest-China and
Tibet are particularly at risk. In Europe, human infections occur
predominantly in the south and east [3, 4].
In Germany cystic echinococcosis was known to be transmitted
autochthonously until the sixties. Nowadays, however, cystic
echinococcosis is perceived as an infection of migrants acquired
in their countries of origin. Established transmission cycles are
considered to have been interrupted in Germany by the improvement
of hygiene in slaughterhouses, preventing the access of dogs
to infected organs of slaughtered animals. Sporadically, cystic
echinococcosis is registered in German individuals, but the high
mobility of the population and the long-lasting pre-symptomatic
phase precludes the possibility of reconstructing where the infection
had been acquired.
At present, it is not clear, whether or not transmission of cystic
echinococcosis to humans still occurs in Germany. Since 2001,
cases of cystic echinococcosis are a mandatorily notifiable disease
that needs to be reported to the Robert Koch-Institut (RKI, German
national public health institute). Between 2001 and 2007 some
413 of notified cases were identified as new infections. Notifying
doctors communicated the most probable source of infection in
296 of these 413 cases. Among these 296 cases more than one
sixth (56 cases) of infections were deemed as having been acquired
in Germany [5]. Therefore, we attempted to identify particular risks
and the most probable source of infection by conducting a survey
among patients with cystic echinococcosis who grew up in Germany.
Patients, materials and methods
Patients were recruited among individuals diagnosed with cystic
echinococcosis, who grew up in Germany, and attended our regional
referral centers in Germany, between 1999 and 2008. Patients
were given detailed information on the study and asked for their
consent to participate. Criteria for the definite diagnosis of cystic
echinococcosis were imaging findings (ultrasound, computerized
tomography and magnetic resonance imaging) showing a typical
morphology for cystic echinococcosis. The findings were,
classified according to the recommendations of the World Health
Organization (WHO) - Informal Working Group on Echinococcosis
[6]. Patients with transitional partially solidified cysts (WHO-CE
4) are sometimes difficult to diagnose on imaging findings alone:
these cases were only included when other parameters (histology,
detection of hooks or protoscolices in cystic fluid, antibodies to
E. granulosus) supported or confirmed the imaging findings [7-9]
(Table). Treatment and follow up were performed according to the
stage of the disease [3,7,9].
Patients were asked to answer a detailed questionnaire
concerning their entire life history and living conditions in all
places where they had lived, with emphasis on urban or rural
environment, dog contacts, whether they knew if slaughtering was
controlled or not in the area they lived, and possibilities of an
accidental transportation of parasite ova from dog faeces to raw
food by cockroaches or flies. Patients were asked to present a
detailed life-long travel history answering the same questions as in
the questionnaire above. Where patients reported contacts to dogs,
information on the origin and history of displacements of the dogs
was also obtained.
Results
History of exposure
Twentytwo patients with cystic echinococcosis, who had grown
up in Germany, were recruited for the survey. Seven of them were
excluded because their data were incomplete. The 15 remaining
German cystic echinococcosis patients, seven female, eight male,
were able to give exhaustive information to answer the questionnaire.
Their age at the date of diagnosis was 16 to 68 years (median 48
years). Detailed results on their history of travel and exposure to
dogs and findings (laboratory and imaging) are shown in the Table.
Since patients were uncertain about possible transmission risks,
other than the two mentioned above, the cumulative duration of
dog contacts in and outside Germany was defined as the best
measurable risk factor.
Only two patients (n° 4 and n° 6) did not recall contacts with
dogs. These two patients mainly had lived in Germany, although
one patient (n° 4) had stayed for some months in a high risk area,
Northern Africa, the other patient (n° 6) had travelled in areas with
a high incidence of cystic echinococcosis only on holidays.
Among the patients who recalled having been in contact with
dogs, one patient (n° 9) reported an extended stay in a rural area
of central Italy, where he had kept dogs. For many years he also
owned dogs in Germany.
Two patients (n° 13 and n° 14) had never left Germany even
for short periods. For 10 patients the cumulative time of exposure
to dogs was longest in Germany. One of them, patient n° 11, had
imported his dog from Hungary to Germany, whereas the others
had been exposed to local dogs only. Some of the latter patients
may have also occasionally been exposed to cystic echinococcosis
outside Germany, such as patient n° 8, a medical doctor, who had
worked in Brazil for four years. However, he had lived in an area
of very low endemicity and he did not recall any contact with local
dogs there [4; 10]. Although patient n° 7 had lived for some time in
highly endemic regions he did not remember any contact with dogs
during these stays. Five of the patients reported only short holidays
in endemic countries but did not remember any contact with local
dogs (n° 2, n° 5, n° 10, n° 12, n° 15). Patient n° 3 had taken her
pet dog with her on holidays to Italy (Riccione, Emilia- Romagna).
40
Discussion
Unexpectedly, in the majority of cases included in our study,
infection by a local dog was the most likely explanation of cystic
echinococcosis in patients who grew up in Germany. In two of the
15 cases there is no doubt about autochthonous infection, because
they have never in their life-time travelled outside Germany. Our
hypothesis of autochtonous infection in Germany may be confuted
in some other cases where infection might also be interpreted as
a travel associated disease [11].
The probability of autochthonous transmission depends on the
prevalence of cystic echinococcosis in domestic animals, on the
access of dogs to raw slaughter offal or to infected animal carcasses
and the intensity and duration of contact between dogs and
humans. Dog ownership, in particular the duration of dog ownership
is the best established risk factor for human cystic echinococcosis
[12]. Sometimes, humans may become infected without contact to
dogs; indirect transmission occurs, when arthropods such as flies
or cockroaches or birds transport ova of E. granulosus from dog
excrements on raw food, e.g. salad [12-18]. In a rural environment,
small children may also become infected when they accidentally
ingest ova after crawling on the floor which has been contaminated
by excrements of an infected dog. The type of water supply (i.e.
tap water, wells) has also been suggested to be associated with
the risk of human cystic echinococcosis. In a highly endemic rural
area of Kazakhstan five out of 120 selected soil samples contained
eggs of E. granulosus [19]. Obviously, no patient in our series
could exclude these conceivable indirect ways of transmission.
Indirect transmission most likely accounts for those two of our
patients who did not recall any dog contact and may account for
some other case, although an occasional dog contact which has
been forgotten cannot be ruled out completely. However, the risk of
indirect transmission by such sporadic events appears to be much
lower than a long-lasting contact to a dog that is harbouring adult
worms and thus constantly excreting worm ova over a time period
of up to 22 months [10, 12-18].
Unfortunately, in Germany reliable data on the actual prevalence
of cystic echinococcosis in domestic animals are not available.
Infections of cattle were sporadically reported in Germany until
the nineties [10; 20]. The prevalence of E. granulosus infections
in dogs is assumed to be very low. The only vertical analysis
available revealed 43 E. multilocularis cases but no E. granulosus
confirmed by molecular analysis out of more than 21,000
specimens of dog excrements sent by Veterinary Medical Clinics
to a German Veterinary Medicine laboratory in 2004 and 2005
[21]. This observation, however, cannot be taken as representative,
because it can be assumed that rural free raging dogs are grossly
underrepresented in this sample.
Controlled slaughtering and inspection of meat, as well as
routine deworming of dogs have contributed to an almost complete
disappearance of E. granulosis in Germany and many neighbouring
countries. However, active foci are still present in countries close
to Germany and frequently visited by Germans such as Poland and
the Mediterranean countries [10; 20; 22].
A persistence of a reservoir of cystic echinococcosis in Germany
cannot be excluded and new risks may arise, such as importation
of infected dogs from endemic areas without deworming as well
as the illegal slaughtering of domestic animals. Recently the reintroduction of cystic echinococcosis to slaughterhouses of a non-
endemic country has been observed in the Netherlands, where
infected cattle had been imported from Romania [23].
As a possibility to more reliably identify the sources of human
cystic echinococcosis in Germany, genetic investigations of the
parasite could be helpful. In former times, cystic echinococcosis
of domestic animals in Germany most frequently occurred in cattle.
It can therefore be assumed that cystic echinococcosis in Germany
was due to the genetically distinct cattle strain (G5 or E. ortleppi).
An old persisting endemicity would be due to this agent. Genotypic
analysis could indicate the origin of the infectious agent: sheepand buffalo strains (G1/G3) are endemic in the Mediterranean
region, and the pig strain (G7 or E. canadensis) is endemic in
eastern Europe [9; D’Amelio, personal communication, 2007].
The actual risk of transmission is very difficult to determine
because of the very slow development and persistence of cysts
in patients for years or even decades. Considering the size and
morphology of the cysts in our patients, infection must have taken
place many years before diagnosis. The two older patients, who
had never travelled outside Germany and who had inactive cysts,
might have been infected in a period before cystic echinococcosis
control had been completely achieved in Germany. This view may
be supported by observations from other countries where cystic
echinococcosis had been eradicated in animals but cysts were
found in humans for many years after transmission had been
interrupted [24,25]. To fully exclude sporadic infection acquired in
endemic regions in the younger patients is impossible. Nowadays, it
is difficult to find young Germans who have never travelled abroad
and infections which are transmitted at present will most probably
be discovered in humans only after years or even decades.
Furthermore, false negative serology results occur frequently,
especially in young cysts (WHO-CL, WHO-CE1) and inactive cysts
(WHO-CE5) [3, 6-10, 13, 17, 26, 27]. Obviously, laboratory
notifications miss those cases where specific antibodies are not
yet detectable. An inquiry among German pathologists showed a
number of approximately 70 new cases of cystic echinococcosis
detected each year, between 1995 and 2001 [28]. In our series,
histopathology had been performed in less than half of the cases.
Moreover, some cases of cystic echinococcosis in German patients
may be misclassified as alveolar echinococcosis, because the
notion that alveolar echinococcosis is endemic in Germany is
common, whereas cystic echinococcosis is considered a disease
of migrants. Reporting clinicians may also overestimate risks of
acquiring cystic echinococcosis abroad because they believe that it
cannot be transmitted in Germany. Thereby, cystic echinococcosis
cases estimated of having been acquired in Germany are likely
to be underreported. Furthermore, differential diagnosis between
congenital cysts and cystic echinococcosisis is sometimes difficult
[29]. Finally, many medical doctors in Germany are not yet
sufficiently familiar with the notification procedures and these
have not found their place in medical routine. Therefore, the
real number of cystic echinococcosiscases is likely to exceed the
number of notified cases. This notion is supported by a recent study
on alveolar echniococcosis where a threefold higher incidence was
found compared with the national surveillance figures [30].
The main limitations of our study are the impossibility to
retrospectively assess transmission risks besides dog contacts and
the high mobility of Germans with frequent stays and holidays
in endemic areas. Nevertheless, despite of these difficulties, it
must be acknowledged that autochthonous transmission of cystic
echinococcosis in our patient series had occurred without doubt
at least in two of 15 cases investigated and that the cumulative
duration of dog contacts in the majority of the remaining patients
was highest within Germany.
At present it is not possible to assess the actual risk of cystic
echinococcosis transmission in Germany. The difficulties arise
from: the very long delay between infection and diagnosis; the
permanence of (apparently) inactive cysts which do not cause
symptoms for years or even decades, insufficient data on the
frequency of cysts found in slaughtered animals including the
possible practice of uncontrolled slaughtering, and insufficient data
on the incidence of E. granulosus infection in local dogs.
Conclusions
Cystic echinococcosis is a worldwide zoonosis, which occurs
sporadically also in Germany. The results of our study strongly
support the notion that a significant proportion of the sporadic
infections are due to autochthonous transmission in Germany,
although cystic echinococcosis may also be acquired from dogs
imported from a region of high endemicity or during a stay in a
highly endemic region. The retrospective design of our study does
not permit an estimation of the actual risk of transmission of cystic
echinococcosis in Germany. However, new threats have to be taken
into account. The European Union is expanding and animal imports
are likely to increase especially from highly endemic countries in
Europe. Epidemiological figures on the actual transmission are
difficult to obtain. Therefore, compulsory notification of human
cystic echinococcosis is one instrument for surveillance that has to
be maintained. Regular inquiries in veterinary medicine laboratories
and slaughterhouses, investigation of dogs at risk of infection as
well as genetic investigations on the strain or species of the causal
agent of cystic echinococcosis are also justified.
A ck now led gem e nts
We thank the patients for their enthusiastic support. The Paul-EhrlichSociety of Chemotherapy supported the establishment of the German
Echinococosis Registry in Ulm, Germany. This work is part of medical
theses by A Orhun and B Just.
References
1. Kern P, Bardonnet K, Renner E, Auer H, Pawlowski Z, Ammann RW et al. European
Echinococcosis Registry. European echinococcosis registry: human alveolar
echinococcosis, Europe, 1982-2000. Emerg Infect Dis. 2003;9(3):343-9.
2. Schweiger A, Ammann RW, Candinas D, Clavien PA, Eckert J, Gottstein B et al.
Human alveolar echinococcosis after fox population increase, Switzerland.
Emerg Infect Dis. 2007;3(6):878-82.
3. Kern P, Reuter S, Kratzer W, Buttenschoen K. Treatment of cystic echinococcosis.
Dtsch Med Wochenschr. 2001;19;126(3):51-4.
4. Romig T, Epidemiology of echinococcosis, Langenbecks Arch Surg. 2003;388:
209-17
5. Robert Koch-Institut. Infektionsepidemiologisches Jahrbuch meldepflichtiger
Krankheiten 2001-2007. ( yearbooks of epidemiology of infections in Germany).
Available from: http://www.rki.de/cln_100/nn_196322/DE/Content/Infekt/
Jahrbuch/jahrbuch__node.html?__nnn=true
6. World Health Organization (WHO). Puncture Aspiration Injection and Reaspiration – an option for the treatment of cystic echinococcosis. WHO
Informal Working Group on Echinococcosis (WHO-IWGE) 2001; WHO/CDS/CSR/
APH/2001. Available from: http://whqlibdoc.who.int/hq/2001/WHO_CDS_CSR_
APH_2001.6.pdf
7.
Junghanss T, da Silva AM, Horton J, Chiodini PL, Brunetti E. Clinical management
of cystic echinococcosis: state of the art, problems, and perspectives. Am J
Trop Med Hyg. 2008;79(3):301-11.
8. Wellinghausen N, Kern P. A new ImmunoCAP assay for detection of Echinococcus
multilocularis-specific IgE. Acta Trop. 2001; 79(2): 123-7.
9. Kern P. Echinococcus granulosus infection: clinical presentation, medical
treatment and outcome. Langenbecks Arch Surg. 2003;388(6): 413-20.
10. Eckert J, Schantz PM, Gasser RB, Torgerson PR, Bessonov AS, Movsesian SO, et
al. Geographic distribution and prevalence. In: Eckert J, Gemmell MA, Meslin
FX, Pawlowski ZS (eds.): WHO/OIE manual on echinococcosis in humans and
animals: a public health problem of global concern. World Organization for
Animal Health 2001, Paris, pp. 100-142, 265. Available from: http://whqlibdoc.
who.int/publications/2001/929044522X.pdf
11. Brunetti E, Gulizia R, Garlaschelli AL, Filice C. Cystic echinococcosis of the
liver associated with repeated international travels to endemic areas. J
Travel Med. 2005; 12(4):225-8.
12. Larrieu EJ, Costa MT, del Caprio M, Moguillansky S, Bianchi G, Yadon ZE. A
case-control study of the risk factors for cystic echinococcosis among the
children of Rio Negro province, Argentina. Ann Trop Med Parasitol. 2002;96(1):
43-52.
13. Brunetti E, Filice C, Genchi, C. Genere Echinococcus in: de Carneri I edt.
Parassitologia generale e umana. Casa Editrice Ambrosiana 13th edition, 2004,
Milan Italy. pp.:317 – 329.
14. Torgerson PR, Karaeva RR, Corkeri N, Abdyjaparov TA, Kuttubaev OT, Shaikenov
RS. Human cystic echinococcosis in Kyrgystan: an epidemiological study. Acta
Trop. 2003;85(1): 51-61
15. Dowling PM, Abo-Shehada MN, Torgerson PR. Risk factors associated with
human cystic echinococcosis in Jordan: results of a case-control study. Ann
Trop Med Parasitol. 2000;94(1):69-75.
16. Dowling PM, Torgerson PR. A cross-sectional survey to analyse the risk factors
associated with human cystic echinococcosis in an endemic area of midWales. Ann Trop Med Parasitol. 2000;(3)94:241-5.
17. Carmona C, Perdomo R, Carbo A, Alvarez C, Monti J, Grauert R et al. Risk factors
associated with human cystic echinococcosis in Florida, Uruguay: results of
a mass screening study using ultrasound and serology. Am J Trop Med Hyg.
1998;58(5):599-605.
18. Wang Q, Qiu JM, Schantz P, He JG, Ito A, Liu FJ. Investigation of risk factors
for development of human hydatidosis among household raising livestock in
Tibetan areas of Western Sichuan province. Zhongguo Ji Sheng Chong Wue
Yu Ji Sheng Chong Bing Za Zhi 2001;19(2): 93-6.
19. Shaikenov BS, Rysmukhambetova AT, Massenov B, Deplazes P, Mathis A,
Torgerson PR. Short report: the use of a polymerase chain reaction to detect
Echinococcus granulosus (G1 strain) eggs in soil samples. Am J Trop Med Hyg.
2004;71(4):441-3.
20. Romig T, Dinkel A, Mackenstedt U. The present situation of echinococcosis in
Europe. Parasitolog y Int. 2006;55 Suppl:S187 – 191.
21. Dyachenko V, Pantchev N, Gawlowska S, Vrhovec MG, Bauer C. Echinococcus
multilocularis infections in domestic dogs and cats from Germany and other
European countries. Vet Parasitol. 2008;157(3-4):244-253.
22. Montinaro L, Sisinni AG, Sartorelli P. L’echinococcosi: un’endemia persistente.
G Ital Med Lav Ergon. 2004;26(3):202-7.
23. Aalten M, Züchner L, Bruinier E, Holzhauer M, Wouda W, Bergsteede F et
al.. Reintroduction of E. granulosus by import of cows in the Netherlands.
Tijdschr Diergeneeskd. 2008;133(21): 898-902.
24. Beard T.C. The elimination of echinococcosis from Iceland. Bull World Health
Organ. 1973;48(6):653-60.
25. Koea JB. Cystic lesions of the liver: 6 years of surgical management in New
Zealand. N Z Medical J. 2008;121(1277): 61-9.
26. Gavidia CM, Gonzalez AE, Zhang W, McManus DP, Lopera L, Ninaquispe B, et al.
Diagnosis of cystic echinococcosis, central Peruvian highlands. Emerg. Inf
Dis. 2008;14,(2):260-6.
27. Hosch W, Junghanss T, Werner J, Düx M: Imaging methods in the diagnosis and
therapy of cystic echinococcosis. Rofo. 2004;176(5):679-87
28. Mohlitz U, Junghanss T, Razum O. Zystische Echinokokkose: eine Befragung
von Pathologen dient der Surveillance und führt zu praktischen
Schlussfolgerungen. RKI Epidemiologisches Bulletin 2005;38: 347 – 349,
Germany.
29. Grüner B, Kratzer W, Buttenschön K, Kern P, Reuter S. A case of sporadic
Echinococcus granulosus infection originary from Southern Germany.
Infection. 2008;36(1):78-81.
30. Jorgensen P, an der Heiden M, Kern P, Schöneberg, Krause G, Alpers K.
Underreporting of Human Alveolar Echinococcosis, Germany. Emerg Infect
Dis. 2008;14 (6):935-7.
Citation style for this article: Richter J, Orhun A, Grüner B, Müller-Stöver I, Reuter
S, Romig T, Häussinger D, Kern P. Autochthonous cystic echinococcosis in patients who
grew up in Germany. Euro Surveill. 2009;14(22):pii=19229. Available online: http://www.
42
6
41 female
5
38 male
4
38 male
3
27 female
2
19 female
1
16 female
Patient-n°.
age at date of
diagnosis ( years)/ sex
(m = male, f = female)
3 weeks
1 week
1 week
41 years
3 weeks
3 weeks
3 weeks
3 weeks
Libanon
Tunesia
Germany (rural)
Spain (Canarian
Islands)
Mediterranean
Yugoslavia (beach)
Italy(beach)
38 years
Germany (rural)
10 weeks
10 weeks
Japan
Turkey
5 months
United States
6 months
Northern Africa±±
38 years
Germany
Newzealand
3 weeks
Italy (beach)
22 years
Germany
3 weeks
2 weeks
Morocco
Croatia(beach)
2 weeks
19 years
Germany (rural))
Italy (Sardinia)
3 weeks
16 years
None
None
None
None
None
None
None
None
None
Yes
None
None
None
None
None
None
None
None
None
None
None
None
1872
None
None
None
None
3
None
None
Brought her pet along
from Germany
988
None
None
Own dogs
None
None
988
Dogs in the
neighbourhood
None
n.a.
n.a.
None
Mild
abdominal
discomfort
Diagnostic findings
Accidentally by ultrasound
By ultrasound because of
abdominal complaints
Accidentally by a
posttraumatic ultrasound
after a ski accident
≤400/μl
≤4%
≤400/μl
≤4%
≤400/μl
≤4%
282/μl
3.0%
100/μl
1.9%
≤400/μl
≤4%
≤100
≤100
33.5
18
365
≤100
Positive
Positive
Positive
Positive
Positive
negative
n.a.
n.a..
n.a.
Positive
n.a.
n.a.§
Eosinophils/
IgE
Serology
Conditions of discovery of μl (normal
Serology
IHA*
Cystic echniocccois
≤400); (normal (IU/ml)
ELISA†
-1)
(normal≤100)
(<32
≤4%)
Severe back performed during a
pain
dissection of a renal
artery
None
Abdominal
discomfort
None
Cumulative
duration
Clinical
of pet
symptoms
contacts
(weeks)
Frequent visit to
grandparents who
slaughtered domestic
832
animals at home. Grand
father also had CE
Cumulative
duration of Pet contact
stay
Italy
Germany (rural)
Countries of
exposure
History of exposure
Demographic data, history of exposure, clinical symptoms and findings prior to diagnosis in patients with cystic echinococcosis who grew up in Germany
Ta b l e
Liver cyst CE 5
active Liver
cyst
Ruptured liver
cyst with
bacterial
superinfection
Histopatholog y
positive
IgE-CAP-RAST specific Multiple liver
for CE: 1
cysts
IgE-CAP-RAST specific
for CE: 0
Histopatholog y
positive
for CE: 1
Liver cyst CE4
Western-Blot positive
# CBR neg
**IFT neg
Histopatholog y
positive
Histopatholog y
positive
for CE¶
Liver cyst CE 1
Histopatholog y
positive
Other investigations Imaging±
44
11
63 male
10
60 female
9
50 male
8
48 male
7
47 male
4 months
60 years
Once yearly
for 1-3
None
weeks each
Germany (rural)
Austria (rural)
5 days
7 days
5 days
Greece (beach)
Netherlands
Yugoslavia (beach)
2 weeks
Hungary
(hunting)
7 days
41 years
Germany (mostly
rural)
Portugal (beach)
2 weeks
Greece
12 days
2 weeks
Turkey
2 weeks
2 weeks
France
France (urban)
2 weeks
Netherlands
Austria (hunting)
None
2 weeks
Switzerland
None
Yes
None
None
None
Yes, own dog imported
from Hungary
Yes
None
None
None
None
None
Spain (Canary Islands) 2 weeks
Dog of her brother
Yes
6 years
Spain (rural)
Yes
Yes
None
None
Yes
None
None
None
None
None
None
Yes
Italy (rural)
37 years
34 years
Germany (partially
rural)
Germany (rural)
1 Monat
Russia (urban)
2 months
1 month
Greece (rural)
Portugal (urban)
1 month
Nigeria (rural)
4 years
2 months
France (rural)
Brazil (urban)
8 months
4 years
Netherlands (rural)
Peru (rural)
18 years
Germany (rural)
None
1
None
None
None
2
624
(contact
Continued
in
Germany)
1334
None
None
None
None
None
None
None
780
18
312
1508
None
None
312
None
None
None
None
None
None
936
Dyspnea
None
Mild
abdominal
discomfort
Cough
None
performed for differential
diagnosis of acute atrial
fibrillation
Chest X ray performed
because of coughing
revealed a pulmonary
shadow
performed because of
abdominal pain due to
acute appendicitis
≤200 / μl
≤2,1%
≤100 μl
≤2.5%
≤100 / μl
≤0.9%
≤900 / μl
≤20,4%
≤200 / μl
≤4.4%
19
6
184
3940
211
Negative
Negative
Negative
Positive
Negative
Positive
Positive
Negative
Positive
Negative
Liver cyst CE 2
Calcified
spleen cyst
Liver cyst CE 4
Western-Blot Positive lLng cyst
Histopatholog y
liver cyst CE 3
Positive
Calcified
kidney cysts,
calcified
spleen cysts
None
None
Republic of South
Africa (beach)
2 weeks
None
3 weeks
Yes
Yes
Spain (Canary Islands, 3 weeks
beach)
India (holiday trip)
26 years
67 years
Yes
None
None
Yes
None
None
None
1144
2964
3328
None
None
728
None
Abdominal
discomfort
None
None
Accidentally by a
posttraumatic ultrasound
screening after a ski
accident
Increased liver enzymes
during routine screening
Epigastic pain,, palpable
abdominal mass
Accidentally by radiology
showing a splenic
calcification
130
10,3
≤55,7 / μl
≤1%
≤100 / μl
≤3,4%
46
38
≤200 / μl
≤3,4%
≤100 / μl
≤1,1%
Positive
Positive
Positive
Negative
Positive
Positive
Negative
ND********
Multiple
iver cysts
in different
development
stages
Western Blot positive Liver cyst CE 5
for CE: 3
Histopatholog y
Positive, Microscopy
of cyst fluid (hooks,
protoscolices)
Liver cysts
CE 1
Calcified
spleen cyst
±± Areas of high endemicity include: Mediterranean countries such as Portugal, Spain, Central and Italy,(southern part, Sardinia and Sicily,), France (southern part), former Yugoslavia including Croatia, Greece, Turkey,
Lebanon; Northern Africa; Kazakhstan, Kyrg yzstan, Nepal, parts of China.
Areas of intermediate endemicity include: parts of Central Europe (Hungary, parts of France), South America, India, West Africa, southern Africa.
Areas with sporadic cases reported: Central Europe (Germany, Switzerland, Austria, Benelux, Scandinavia, United States, Mexico [4,10,12-18,20,22,26]
n.a. = not available,
IHA = immuno haemagglutination,
† ELISA = enzyme-linked immunosorbent assay
±Imaging: classification of liver cysts according to WHO [6];
CE = cystic echinococcosis,
§ n.a.*¶ CAP RAST = radioallergosorbent test [8];
#CBR = complement binding reaction,
** IFT = immunofluorescence test
††ND = not done
15
68 male
Germany (rural)
Germany (rural)
14
67 female
67 years
8 days
Germany (rural)
8 days
Italy (rural)
66 years
Spain (rural)
13
67 male
12
66 female
Germany (rural)

Volume 14, Issue 22 - 4 June 2009

Transcript

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