﻿LETTERS
1120 Emerging Infectious Diseases · www.cdc.gov/eid · Vol. 13, No. 7, July 2007
Qiao-Ping Wang,*
Xiao-Guang Chen
and Zhao-Rong Lun*
*Sun Yat-Sen (Zhongshan) University,
Guangzhou, People's Republic of China;
and Southern Medical University, Guang-
zhou, People's Republic of China
References
1. Xu HG, Qiang S. Inventory invasive alien
species in China. Beijing: Chinese Envi-
ronmental Science Press; 2004.
2. Zhou XC. Risk analysis of invasive Poma-
cea canaliculata. Jian Yan Jian Yi Ke Xue.
2004;14:37­9.
3. Tsai HC, Liu YC, Kunin CM, Lai PH, Lee
SS, Chen YS, et al. Eosinophilic meningi-
tis caused by Angiostrongylus cantonensis
associated with eating raw snails: correla-
tion of brain magnetic resonance imaging
scans with clinical findings. Am J Trop
Med Hyg. 2003;68:281­5.
4. Tsai HC, Liu YC, Kunin CM, Lee SS,
Chen YS, Lin HH, et al. Eosinophilic
meningitis caused by Angiostrongylus
cantonensis: report of 17 cases. Am J
Med. 2001;111:109­14.
5. Lin W, Wang XT. Epidemiological survey
of angiostrongyliasis in Mainland China.
Chin J Zoonoses. 2004;20:1004­5.
6. Hollingsworth RG, Cowie RH. Apple
snails as disease vectors. In: Joshi RC,
Sebastian LC. Global advances in ecology
and management of gloden apple snails.
Nueva Ecija: Philippine Rice Institute;
2006. p. 121­32
7. Chen XG, Li H, Lun ZR. Angiostrongyli-
asis, mainland China. Emerg Infect Dis.
2005;11:1645­7.
8. The number of the case of angiostron-
gyliasis caused by eating P. canaliculata
reached 131 in Beijing. [cited 2007 Jan
21]. Available from http://news3.xinhua-
net.com/fortune//2006-09/12/content_
5078790.htm
9. Cowie RH. Apple snails (Ampullariidae)
as agricultural pests: their biology, im-
pacts and management. In: Barker GM.
Molluscus as crop pests. Wallingford
(UK): CABI Publishing; 2002. p. 145­92
10. Tsai HC, Lee SS, Huang CK, Yen CM,
Chen ER, Liu YC. Outbreak of eosino-
philic meningitis associated with drinking
raw vegetable juice in southern Taiwan.
Am J Trop Med Hyg. 2004;71:222­6.
Address for correspondence: Zhao-Rong
Lun, Center for Parasitic Organisms, State
Key Laboratory of Biocontrol, School of Life
Sciences, Sun Yat-Sen (Zhongshan) University,
Guangzhou 510275, People's Republic of
China; email: lsslzr@mail.sysu.edu.cn
Possible Avian
Influenza (H5N1)
from Migratory
Bird, Egypt
To the Editor: Wild migratory
birds are reservoirs for low pathogenic
avian influenza (LPAI) viruses (1), but
their role in transmitting highly patho-
genic avian influenza (HPAI) viruses
is hotly debated and unclear (2­4). Be-
ginning in July 2005, a clade of HPAI
(H5N1) viruses rapidly expanded from
an apparent focus in western People's
Republic of China and spread to the
Middle East, Africa, and Europe (5).
Genetic analysis of HPAI virus iso-
lates from dead wild birds along major
flyways indicated that the strains were
closely related to the Qinghai H5N1
A/bar-headed goose/Qinghai/65 /2005
virus (clade II) (GenBank accession
no. DQ095622). In addition to trans-
mission to domestic poultry, HPAI
(H5N1)­infected mute swans have
been implicated in direct transmission
to humans in Azerbaijan (6).
The US Naval Medical Research
Unit No. 3 and the Ministry of Envi-
ronment of Egypt have collaborated
since 2003 in obtaining samples from
migratory birds to detect circulating
influenza viruses. During the 2005­06
migratory birds season, 1,304 migra-
tory birds were sampled from either
live bird markets or cage birds trapped
by fishermen in Port Said, Damietta,
Fayoum, Arish, and Sharm el Sheikh
(online Appendix Figure, panel A,
available from www.cdc.gov/EID/
content/13/7/1120-appG.htm).
A total of 203 cloacal swab sam-
ples were positive for influenzaAvirus
matrix gene when tested by real-time
PCR, and 2 were also positive for the
hemagglutinin 5 (H5) gene by using
specific primers (7). Of the 2 migra-
tory birds positive for the H5 gene, the
first was a common teal (Anas crec-
ca) captured in the Nile Delta region
of Damietta in October 2005 (online
Appendix Figure, panel A). Sequenc-
ing of the H5 gene showed that this
virus was an LPAI most closely re-
lated to strain A/mallard/Bavaria/1/
2005(H5N2) (GenBank accession no.
DQ387854 (2).
In January 2006, an influenza A
H5 virus (weak positive result) was
detected in another common teal
(trapped in a cage by a fisherman)
sampled from the Damietta region
in December 2005 (online Appendix
Figure, panel A). The low viral load,
coupled with the failure to isolate the
virus, precluded the laboratory from
conducting sequence analysis at the
time on the basis of insufficient tem-
plate material. After the outbreak of
influenza A (H5N1) in poultry and
humans in Egypt in February 2006,
additional retrospective attempts to
concentrate RNA were used to as-
sess potential introduction scenarios.
After multiple RNA extractions were
conducted and the RNA was concen-
trated, this specimen was found to be
positive for the neuraminidase 1 (N1)
gene by real-time PCR.
The hemagglutinin gene from
both teal strains was sequenced
(1,596 bp). Sequences were aligned
with other influenza A (H5N1) strains
from Egypt (9 from humans, 5 from
chickens). Twenty other strains with
high similarity and from different lo-
cations were selected by using a Gen-
Bank search algorithm and included in
the alignment.Aphylogenetic analysis
was conducted by using the Kimura
2-parameter model. The LPAI H5 vi-
rus strain was used as an outgroup in
a neighbor-joining phylogenetic tree.
Bootstrap analysis with 500 replicates
of sequence data was also conducted
by using MEGA 3.1 software (8).
Phylogenetic analysis showed
clustering of the HPAI (H5N1) strains
collected from 1 geographic region
(country) (online Appendix Figure,
panel B). All HPAI (H5N1) strains
from Egypt from humans or chickens
analyzed clustered with a bootstrap
supportvalueof98%.Furthermore,the
A/Teal/Egypt/14051-NAMRU3/2006
LETTERS
Emerging Infectious Diseases · www.cdc.gov/eid · Vol. 13, No. 7, July 2007 1121
(H5N1) strain (collected in December
2005; online Appendix Figure, panel
A) is an HPAI and is closely related
to the parent of the group of viruses
isolated in the early 2006 Egypt out-
break, with an average identity of
99.4% with all other strains from
Egypt and a bootstrap support value of
96% (online Appendix Figure, panel
B). Despite the rapid spread of this
clade (Qinghai-like strain) to many
countries, since late 2005, strains ana-
lyzed in this study showed low-level
genetic variation (<2%).
Brown et al. reported that spe-
cies can vary greatly in their response
to HPAI (9). At least in ducks, it ap-
pears that viral shedding is highest in
birds with clinical signs of infection,
and lowest, as seen in the common
teal infected with the HPAI strain in
this study, in birds with subclinical in-
fections. These subclinical infections
may be due to flock immunity from
previous exposure to LPAI H5 virus
or genetic factors. This suggestion is
conceivable in light of the LPAI H5
virus detected in the other teal a few
months earlier.
Such naturally resistant wild birds
might serve as vectors for introduction
of HPAI viruses into new locations.
Data presented herein suggest that an
HPAI virus may have been introduced
into Egypt through a migratory bird.
Whether poultry were infected before
mid-February or the teal was infected
with influenza A (H5N1) virus by a
domesticated species is not unknown.
The low degree of viral shedding in-
dicates that detection of any influenza
A (H5N1) virus in wild birds in a new
region should be immediately fol-
lowed up with efforts to characterize
the virus to control the spread of new
subtypes/strains of HPAI into new lo-
cations.
Acknowledgments
We thank the Egyptian Ministry of
Environment for its continued collabora-
tive efforts in migratory bird surveillance.
This study was supported by the
Department of Defense Global Emerg-
ing Infections System (work unit no.
847705.82000.25GB.E0018).
Magdi D. Saad,*
Lu'ay S. Ahmed,
Mohamed A. Gamal-Eldein,
Mohamed K. Fouda,
Fouda M. Khalil,
Samuel L. Yingst,*
Michael A. Parker,*
and Marshall R. Montevillel*
*US Naval Medical Research Unit No. 3,
Cairo, Egypt; and Ministry of Environment,
Cairo, Egypt
References
1. Alexander DJ. A review of avian influenza
in different bird species. Vet Microbiol.
2000;74:3­13.
2. Munster VJ, Wallensten A, Baas C, Rim-
melzwaan GF, Schutten M, Olsen B, et al.
Mallards and highly pathogenic avian in-
fluenza ancestral viruses, northern Europe.
Emerg Infect Dis. 2005;11:1545­51.
3. Sturm-Ramirez KM, Ellis T, Bousfield B,
Bissett L, Dyrting K, Rehg JE, et al. Re-
emerging H5N1 influenza viruses in Hong
Kong in 2002 are highly pathogenic to
ducks. J Virol. 2004;78:4892­901.
4. Normile D. Avian influenza. Evidence
points to migratory birds in H5N1 spread.
Science. 2006;311:1225.
5. Yingst SL, Saad MD, Felt SA. Qinghai-
like H5N1 from domestic cats, northern
Iraq. Emerg Infect Dis. 2006;12:1295­7.
6. Gilsdorf A, Boxall N, Gasimov V, Agayev
I, Mammadzale F, Ursu P, et al. Two clus-
ters of human infection with influenza
A/H5N1 virus in the Republic of Azerbai-
jan, February-March 2006. Euro Surveill.
2006;11:122­6.
7. Spackman E, Senne DA, Myers TJ, Bulaga
LL, Garber LP, Perdue ML, et al. Devel-
opment of a real-time reverse transcriptase
PCR assay for type A influenza virus and
the avian H5 and H7 hemagglutinin sub-
types. J Clin Microbiol. 2002;40:3256­
60.
8. Kumar S, Tamura K, Nei M. MEGA3: In-
tegrated software for molecular evolution-
ary genetics analysis and sequence align-
ment. Brief Bioinform. 2004;5:150­63.
9. Brown JD, Stallknecht DE, Beck JR, Su-
arez DL, Swayne DE. Susceptibility of
North American ducks and gulls to H5N1
highly pathogenic avian influenza viruses.
Emerg Infect Dis. 2006;12:1663­70.
Address for correspondence: Magdi D. Saad,
Commanding Officer, US Naval Medical
Research Unit No.3, PSC 452, Box 5000, MDS
Code 303, FPO AE 09835-0007, Cairo, Egypt;
email: darwishm@namru3.med.navy.mil
Community-
acquired Extended-
Spectrum
-Lactamase
Producers,
United States
To the Editor: Extended-spec-
trum -lactamase (ESBL)­producing
organisms have become a common
problem for patients in hospitals and
other healthcare facilities (1). Com-
munity-onset ESBL infections have
recently been described in Spain, the
United Kingdom, Israel, and Canada
(2,3). Typically, the infections are uri-
nary tract infections (UTIs) with CTX-
M­producing Escherichia coli. These
organisms may be resistant to most
or all antimicrobial agents commonly
used to treat UTIs, such as ciprofloxa-
cin, trimethoprim-sulfamethoxazole,
gentamicin, and ceftriaxone.
Although CTX-M­producing E.
coli have previously been found in the
United States (4), clinical descriptions
of community-acquired ESBL-pro-
ducing E. coli infections have not been
reported in this country. We describe 2
healthy young women in Pennsylvania
in whom UTI with CTX-M-15­pro-
ducing E. coli developed.
A 25-year-old woman was seen
in October 2006 at the emergency de-
partment of a hospital in Pittsburgh
reporting frequent urination, chills,
and bilateral back pain. She had no
relevant past medical history except
for previous UTIs. Results of a physi-
cal examination were unremarkable.
