Browse the corpus

To the Editor: The proposal by Stringer et al. to change the name of Pneumocystis carinii found in humans to Pneumocystis jirovec requires critical consideration (1). First, their rationale for the choice of Jírovec is not compelling. Principle III of the International Code of Botanical Nomenclature (ICBN) states: “the nomenclature of a taxonomic group is based upon priority of publication” (2). Jírovec’s publication in 1952 was not the first to report P. carinii infection in human lungs. In 1942, two Dutch investigators, van der Meer and Brug, described P. carinii as the infecting organism in a 3-month-old infant with congenital heart disease and in 2 of 104 autopsy cases (a 4-month-old infant and a 21-year-old adult) (3). Their description, photomicrographs, and drawings of P. carinii are unequivocal. They also described the typical “honeycomb” patterns in alveoli. In 1951, Dr. Josef Vanek at Karls-Universität in Praha, Czechoslovakia, reported his study of lung sections from 16 children with interstitial pneumonia and demonstrated that the disease was caused by P. carinii (4). Vanek notes in his report, “In man the parasite was for the first time established as a cause of pneumonia in a child by G. Meer and S. L. Brug (1942).” In 1952, Jírovec reported P. carinii as the cause of interstitial plasmacellular pneumonia in neonates (5). A year later, in a coauthored publication, Vanek, Jírovec, and J. Lukes acknowledged and referenced the earlier reports of van der Meer and Brug and Vanek (6). If principle III is to be followed, as well as fairness to the investigators, both van der Meer and Brug and Vanek hold priority over Jírovec, assuming the designation of the species name should be based on the name of the first person to discover P. carinii in humans.

er reports of van der Meer and Brug and Vanek (6). If principle III is to be followed, as well as fairness to the investigators, both van der Meer and Brug and Vanek hold priority over Jírovec, assuming the designation of the species name should be based on the name of the first person to discover P. carinii in humans. The nomenclature of P. carinii has actually been fraught with errors from the beginning. In the earliest publications, Carlos Chagas and Antonio Carini mistook the organism for stages in the life cycle of trypanosomes. Chagas placed it in a new genus, Schizotrypanum (7,8). In 1912, Delanoë and Delanoë at the Pasteur Institute in Paris published the first description of the organism as a new entity unrelated to trypanosomes (9). They proposed the name “Pneumocystis carinii” as a tribute to Carini. The Delanoë paper has remained unchallenged as the original description of P. carinii. Both Chagas and Carini later acknowledged their errors and the validity of the Delanoës’ conclusion. By current ICBN principles, P. carinii is acceptable nomenclature because the authors of the first publication proposed the name of Carini, rather than their own.

unchallenged as the original description of P. carinii. Both Chagas and Carini later acknowledged their errors and the validity of the Delanoës’ conclusion. By current ICBN principles, P. carinii is acceptable nomenclature because the authors of the first publication proposed the name of Carini, rather than their own. In addition, changing the name to P. jiroveci will create confusion in clinical medicine where the name P. carinii has served physicians and microbiologists well for over half a century. I was moved to write this letter because of a call from a knowledgeable oncologist asking for information on “the new strain of P. carinii that has just been reported from the Centers for Disease Control and Prevention,” referring to the report by Stringer et al (1). AIDS patients are well informed about P. carinii pneumonia and avidly monitor medical news about their disease. Without doubt, the name change will cause confusion and undue anxiety among the many thousands of HIV-infected patients who attend clinics. Health-care workers will have an added burden of explaining why the name was changed, but the organism and infection are unchanged. Also, versions of the pronunciation of jiroveci (yee row vet zee) by American patients, physicians, and health-care workers will be interesting to hear.

fected patients who attend clinics. Health-care workers will have an added burden of explaining why the name was changed, but the organism and infection are unchanged. Also, versions of the pronunciation of jiroveci (yee row vet zee) by American patients, physicians, and health-care workers will be interesting to hear. The tone of the article by Stringer et al. implies that the change of P. carinii to P. jiroveci is final, which is not the case. The nomenclature of fungi is governed by ICBN under the auspices of the International Botanical Congress and is not based solely on molecular genetics. Neither P. carinii nor P. jiroveci have been submitted for ICBN scrutiny. In another paper, Stringer et al. outline the mechanics for submission, but indicate that no application has been submitted for their proposal (10). In fact, P. carinii has not been acknowledged as a fungus by ICBN or any other authoritative taxonomic system. Only when nomenclature is registered in ICBN, can a name be referred to as “formally accepted.” In the meantime, the workable terminology proposed earlier by Stringer et al. in 1994 (11) will suffice for clinical use.

P. carinii has not been acknowledged as a fungus by ICBN or any other authoritative taxonomic system. Only when nomenclature is registered in ICBN, can a name be referred to as “formally accepted.” In the meantime, the workable terminology proposed earlier by Stringer et al. in 1994 (11) will suffice for clinical use. Emerg Infect DisEIDEmerging Infectious Diseases1080-60401080-6059Centers for Disease Control and Prevention 02-071110.3201/eid0902.020711Letters to the EditorStringer James R. *Ben Beard Charles †Miller Robert F. ‡Cushion Melanie T. ** University of Cincinnati, Cincinnati, Ohio, USA† Centers for Disease Control and Prevention, Atlanta, Georgia, USA‡ University College London, London, UKAddress for correspondence: Charles Ben Beard, Centers for Disease Control and Prevention, 1600 Clifton Road, Mailstop F22, Atlanta, GA 30333, USA; fax: 770-488-4258; e-mail: cbeard@cdc.gov2 2003 9 2 276 277 In Response We appreciate Dr. Hughes’ letter of concern regarding our article endorsing the name Pneumocystis jiroveci (1). When working with well-known disease agents and syndromes, these types of changes are more difficult to adopt because of the effect they have on daily communication, patient care, record keeping, and other important routines of health-care providers. However, in this case, new information and understanding dictate that a change be made.

well-known disease agents and syndromes, these types of changes are more difficult to adopt because of the effect they have on daily communication, patient care, record keeping, and other important routines of health-care providers. However, in this case, new information and understanding dictate that a change be made. For some time, scientists have known that humans are infected by a particular species of Pneumocystis and that this species does not infect other host species. In recognition of these facts, Frenkel named the human pathogen Pneumocystis jiroveci, using the procedure prescribed by the International Code of Botanical Nomenclature (ICBN) (2). Although Dr. Hughes raised a number of issues, none justifies rejecting the new, valid name.

s species does not infect other host species. In recognition of these facts, Frenkel named the human pathogen Pneumocystis jiroveci, using the procedure prescribed by the International Code of Botanical Nomenclature (ICBN) (2). Although Dr. Hughes raised a number of issues, none justifies rejecting the new, valid name. Dr. Hughes suggested that the name P. jiroveci is incorrect on the basis of principal III of ICBN, which holds that “the nomenclature of a taxonomic group is based upon priority of publication.” He indicated that Jírovec was not the first investigator to report Pneumocystis in humans. Although this situation may be the case, principal III has not been violated because “priority of publication” refers to the time when a name is validly published, not to the time when an organism is first described. The name P. jiroveci was validly published in 1999, and this name therefore has priority. To be valid, all of the following steps must be completed: a name must be published in a scientific journal, the name must be a binary Latin name, the organism must be described in Latin, the rank of the organism must be indicated, and the new species must be called by the term “typus or holotypus,”and the specimen or microscope slides must be placed in a public holding (details are available from: URL: http://www.bgbm.fu-berlin.de/iapt/nomenclature/code/SaintLouis/0000St.Luistitle.htm). Dr. Frenkel was the first to fulfill these requirements in his 1999 publication (2).

be called by the term “typus or holotypus,”and the specimen or microscope slides must be placed in a public holding (details are available from: URL: http://www.bgbm.fu-berlin.de/iapt/nomenclature/code/SaintLouis/0000St.Luistitle.htm). Dr. Frenkel was the first to fulfill these requirements in his 1999 publication (2). The 1912 publication by Delanoë and Delanoë does not have priority in naming Pneumocystis from humans because the organism studied by the Delanoës was from the rat. The rat-derived Pneumocystis organism continues to be known as P. carinii, in keeping with principal III. As an additional historical note, Dr. Frenkel was the first investigator to understand the clear differences between human and rat-derived Pneumocystis, which were described in a landmark publication in 1976 (3). He proposed a change in nomenclature in which the name Pneumocystis jiroveci n. sp. applied to the human organisms and Pneumocystis carinii was retained for the rat organism. However, Frenkel did not attempt to follow ICBN procedures because at the time Pneumocystis was thought to be a protozoan. Nevertheless, this early paper established the idea of naming human Pneumocystis, P. jiroveci.

veci n. sp. applied to the human organisms and Pneumocystis carinii was retained for the rat organism. However, Frenkel did not attempt to follow ICBN procedures because at the time Pneumocystis was thought to be a protozoan. Nevertheless, this early paper established the idea of naming human Pneumocystis, P. jiroveci. Dr. Hughes stated a concern over the possibility that the name change may cause “confusion and undue anxiety among the many thousands of HIV-infected patients who attend clinics.” Such concern is understandable. However, patients will have guidance in understanding the significance of the name change. Health-care providers will allay any fears that might be elicited by the application of the new name. The level of anxiety experienced by persons at risk of acquiring Pneumocystis carinii pneumonia (PCP) is more likely to decline than to increase. People may be relieved to learn that they are not going to catch PCP from a pet, for example.

will allay any fears that might be elicited by the application of the new name. The level of anxiety experienced by persons at risk of acquiring Pneumocystis carinii pneumonia (PCP) is more likely to decline than to increase. People may be relieved to learn that they are not going to catch PCP from a pet, for example. Dr. Hughes suggested that the name P. jiroveci is unofficial because it has not yet been sanctioned by a body of experts that scrutinizes proposed name changes and has the power to either accept or reject them. This situation is not the case. The process by which new names are validated does not directly involve a body of experts. The International Botanical Congress does not evaluate names. Instead, the congress has established ICBN, which sets forth the procedures authors must follow to publish a valid new name. The scientific basis for the new name is included in the publication. In the case of P. jiroveci, abundant evidence shows that P. carinii and P. jíroveci are different species. This evidence, which also indicates that the genus Pneumocystis contains many additional species, has been reviewed extensively (4,5). Dr. Hughes gave the impression that that this evidence is exclusively molecular genetic data. In fact, the molecular genetic evidence is mirrored by clear biologic differences, the most dramatic being host species specificity.

the genus Pneumocystis contains many additional species, has been reviewed extensively (4,5). Dr. Hughes gave the impression that that this evidence is exclusively molecular genetic data. In fact, the molecular genetic evidence is mirrored by clear biologic differences, the most dramatic being host species specificity. As our knowledge of the biology and genetics of disease-causing microorganisms grows, openness to changes in the taxonomy and classification is needed. Given the impact such changes can have outside of the realm of basic science, the decision to accept the proposed changes in the nomenclature used for Pneumocystis has not been made frivolously. This decision is the result of a long and deliberate process that began almost 10 years ago, when data demonstrating that different mammalian hosts harbor different Pneumocystis species first began to appear. In 1994 and 2001, nomenclature issues were discussed at international meetings of the Pneumocystis community, with both physicians and research investigators present. In 1994, the data supporting new species were relatively limited. Consequently, a provisional tripartite nomenclature was adopted in lieu of recognizing new species (6). By 2001, however, the existence of multiple species and the necessity of assigning new species names were accepted by consensus. Because Frenkel had already published the name P. jiroveci, the suitability and validity of this name were also discussed. The new name was approved by consensus (4). We recognize that the results of these meetings do not necessarily reflect all opinions on the matter of Pneumocystis nomenclature, but we know of no better way to assess the majority opinion.

he name P. jiroveci, the suitability and validity of this name were also discussed. The new name was approved by consensus (4). We recognize that the results of these meetings do not necessarily reflect all opinions on the matter of Pneumocystis nomenclature, but we know of no better way to assess the majority opinion. In endorsing the name Pneumocystis jiroveci, we hope to foster scientific understanding and communication. The tripartite name formerly used to denote the distinctness of this organism is not only cumbersome, it is inadequate because its meaning is not apparent and must be defined every time it is used. The arcane nature of the tripartite name tended to deprive the broad audience of persons interested in PCP of vital information, namely, a unique species of Pneumocyctis infects humans. By contrast, the new species name clearly states the uniqueness of P. jiroveci; a distinction is needed when assessing the significance of findings obtained by studies on other members of the genus. Recognition of this uniqueness will undoubtedly stimulate more research on this species. Communication will best be served by uniformity in nomenclature.

e clearly states the uniqueness of P. jiroveci; a distinction is needed when assessing the significance of findings obtained by studies on other members of the genus. Recognition of this uniqueness will undoubtedly stimulate more research on this species. Communication will best be served by uniformity in nomenclature. Frenkel has assigned a valid name to the Pneumocystis species found in humans. Ignoring this name on the grounds of inconvenience is not only unjustified, it is impractical. If names published in accordance with ICBN are not accepted, the field will have no recognized mechanism for conferring names, fostering the use of idiosyncratic, inadequate, and misleading names. Communication and progress will suffer as a result. Furthermore, if we choose to ignore critical changes in taxonomy for subjective reasons, when these changes are mandated by new and indisputable information, then taxonomy itself becomes meaningless and as a consequence, practitioners of public health, clinical medicine, and biomedical research might as well call any disease agent by whatever name they choose.

The continuing spread of H5N1 avian influenza viruses from eastern Asia to domestic and wild birds in central Asian countries, including Mongolia, Kazakhstan, Russia, and Turkey, indicates the extent to which the geographic range of this highly pathogenic influenza virus has expanded. The highly pathogenic H5N1 viruses were first detected in 1996 in geese in Guangdong, China (1); they later spread to ducks in the coastal provinces of South China (2) and to Hong Kong's live poultry markets (3). These viruses infected at least 18 persons in Hong Kong, 6 of whom died (4). The viruses were eradicated in 1998 by the culling of all poultry in Hong Kong and by changing marketing practices. Although these particular genotypes have not been detected again, other H5N1 genotypes continued to emerge in 2000 and 2001 (5).

hese viruses infected at least 18 persons in Hong Kong, 6 of whom died (4). The viruses were eradicated in 1998 by the culling of all poultry in Hong Kong and by changing marketing practices. Although these particular genotypes have not been detected again, other H5N1 genotypes continued to emerge in 2000 and 2001 (5). The biology of the H5N1 viruses changed dramatically for the first time in late 2002, when the viruses were isolated from dead wild aquatic birds in Hong Kong and from decorative waterfowl that died in Kowloon Park, Hong Kong (6,7). After the Z genotype of H5N1 influenza became established as the dominant H5N1 influenza virus in eastern Asia, it was transmitted to persons in Vietnam, Thailand, and Cambodia. In 2004, a distinguishable genotype was transmitted to persons in Indonesia (8). Most human cases have resulted from the direct transmission of virus from poultry to humans (9). To date, evidence for human-to-human transmission is limited (10,11). In Thailand, 13 persons infected with an H5N1 influenza virus died in 2004, and 2 additional human deaths occurred in October 2005. By contrast, in neighboring Vietnam, 42 human deaths caused by H5N1 influenza virus were reported in 2005. What accounts for these differences? Here we examine the hypothesis that the lower death rate in Thailand resulted in part from that government's recognition of the role of backyard chickens and domestic ducks in the spread and perpetration of H5N1 influenza virus and the government's aggressive culling of flocks in which the virus was detected (12).

ces? Here we examine the hypothesis that the lower death rate in Thailand resulted in part from that government's recognition of the role of backyard chickens and domestic ducks in the spread and perpetration of H5N1 influenza virus and the government's aggressive culling of flocks in which the virus was detected (12). Thai health officials recognized that the spread of H5N1 influenza viruses to domestic chickens correlated with the distribution of free-grazing ducks (13). At the beginning of the 2004 poultry outbreak, ducks were raised in 1 of 4 systems: 1) in high-biosecurity closed houses; 2) in moderately high-biosecurity open houses (ducks raised for meat and laying ducks); 3) in rice fields after harvest (free-range or so-called grazing ducks); or 4) in backyards (backyard ducks). We discuss each method, particularly emphasizing the role of grazing ducks in the perpetuation and spread of H5N1 in the country. We also describe the clinical and pathologic changes in ducks and consider the current policies regarding duck raising in Thailand. We conclude that the traditional methods of raising ducks in Thailand and the rest of Southeast Asia must be modified if we are to control the spread of avian influenza virus. Methods of Duck Raising in Thailand Four systems were in use during 2004 (Figure 1).

Thai health officials recognized that the spread of H5N1 influenza viruses to domestic chickens correlated with the distribution of free-grazing ducks (13). At the beginning of the 2004 poultry outbreak, ducks were raised in 1 of 4 systems: 1) in high-biosecurity closed houses; 2) in moderately high-biosecurity open houses (ducks raised for meat and laying ducks); 3) in rice fields after harvest (free-range or so-called grazing ducks); or 4) in backyards (backyard ducks). We discuss each method, particularly emphasizing the role of grazing ducks in the perpetuation and spread of H5N1 in the country. We also describe the clinical and pathologic changes in ducks and consider the current policies regarding duck raising in Thailand. We conclude that the traditional methods of raising ducks in Thailand and the rest of Southeast Asia must be modified if we are to control the spread of avian influenza virus. Methods of Duck Raising in Thailand Four systems were in use during 2004 (Figure 1). Figure 1 Duck-raising systems in Thailand. A) Closed system with high biosecurity, an evaporative cooling system, and strict entrance control. B) Open system but with netting to prevent entrance of passerine birds. Biosecurity was not strictly enforced. This system is no longer approved for the raising of poultry. C) "Grazing duck raising." Biosecurity is never practiced in this system. D) Backyard Muscovy ducks raised for a family; no biosecurity is practiced in this system.

t with netting to prevent entrance of passerine birds. Biosecurity was not strictly enforced. This system is no longer approved for the raising of poultry. C) "Grazing duck raising." Biosecurity is never practiced in this system. D) Backyard Muscovy ducks raised for a family; no biosecurity is practiced in this system. Closed High-Biosecurity System Pekin ducks and white Cherry Valley ducks are raised in closed sheds housing 5,000–6,000 birds each. Day-old ducklings are raised for meat in 50 to 55 days by using an "all-in/all-out" system. Before the ducks are sent to slaughter, 60 cloacal samples (≈1%) are collected for virus isolation. In the slaughterhouse, 60 additional samples are collected from the same flock for virologic analysis. At the end of every 50- or 55-day cycle, each poultry house is cleaned and disinfected. After 3 to 4 weeks, the farm is repopulated with day-old ducklings and the cycle is repeated. In 2005, ≈2–3 million ducks were raised in this system.

e, 60 additional samples are collected from the same flock for virologic analysis. At the end of every 50- or 55-day cycle, each poultry house is cleaned and disinfected. After 3 to 4 weeks, the farm is repopulated with day-old ducklings and the cycle is repeated. In 2005, ≈2–3 million ducks were raised in this system. Open House System In the open house system, ducks are raised for meat or as egg layers. The species raised for meat, Pekin and white Cherry Valley ducks, are raised essentially as in the closed-house system with the all-in/all-out strategy. Virologic sampling is conducted as described above. At present ≈1 million to 2 million ducks are being raised in this system. The species raised as egg layers are khaki Campbell, native laying ducks, and a crossbreed of the khaki Campbell and native laying duck. Layer ducks are housed in flocks of 3,000 to 4,000 birds. After they begin laying eggs (at 5 to 6 months of age), these ducks are kept for 12 to 13 months or until they stop laying, at which point they are sent for slaughter. After a short period for cleaning the houses, additional ducks are added as space becomes available. Presently, ≈5 million to 8 million laying ducks are raised in this system in Thailand. Laying ducks are sampled for virologic analysis every 3 months. Influenza-positive flocks are culled.

t they are sent for slaughter. After a short period for cleaning the houses, additional ducks are added as space becomes available. Presently, ≈5 million to 8 million laying ducks are raised in this system in Thailand. Laying ducks are sampled for virologic analysis every 3 months. Influenza-positive flocks are culled. Grazing System (Free-range Ducks) In 2004, ducks were also raised in the open on rice fields. Most free-range ducks are egg-laying ducks such as khaki Campbell or a crossbreed of khaki Campbell and native laying ducks. However, a small number of "meat" ducks, such as Pekin and white Cherry Valley ducks, are also raised in the open. After hatching and spending 3 weeks in a brooder, young female ducks are moved to rice paddy fields. For the next 5 to 6 months, they grow by eating snails and residual rice after the harvest. When the food supply in 1 field is exhausted, the ducks are moved by truck to another field, often over considerable distances, and even from 1 province to another (Figure 2). When the grazing female ducks are 5–6 months old, they are brought back to the farms, as in the open system described above. However, some flocks of female laying ducks are kept in the rice fields. Male ducks of the species, who are raised with egg-laying hens, and others that are produced for meat are raised in the grazing system for 2 months and are then taken to the slaughterhouses. If they have not reached the optimal weight for slaughter, they are fed supplementary rations for 1 to 2 weeks. During the nationwide surveillance campaign in 2004, 60 cloacal swab samples from each flock were collected for virologic analysis, and the whole flock was culled if a single duck was positive for H5N1 by virus isolation. Flocks that were negative for virus were monitored and put into houses. At the beginning of 2004, ≈10 million to 11 million grazing ducks were being raised in Thailand. Raising free-range ducks is currently illegal in Thailand; all are housed.

flock was culled if a single duck was positive for H5N1 by virus isolation. Flocks that were negative for virus were monitored and put into houses. At the beginning of 2004, ≈10 million to 11 million grazing ducks were being raised in Thailand. Raising free-range ducks is currently illegal in Thailand; all are housed. Figure 2 Example of grazing-duck movement. A single flock of ducks was moved 3 times by truck in 1 season in 2004. The size of the flock is 3,000–10,000. The time spent at each site depends on the availability of rice fields at the site: an acre of rice could support 3,000 ducks for 1 to 2 days. The duck owners have agreements with the landowners regarding the time of harvest and the acreage available. One flock could spend as long as 1 month at a single site before being moved to the next. Backyard Ducks Mixed species of ducks continue to be raised in the backyards of village homes together with other animals, including chickens, geese, and pigs. The duck species raised in backyards include Pekin, white Cherry Valley, Barbary Muscovy, khaki Campbell, native laying ducks, and mule ducks (a sterile crossbreed of Muscovy ducks and native ducks). If a single case of H5N1 infection is detected in a village, all the poultry in the village are culled. Approximately 1.0 million to 1.5 million ducks were raised as backyard ducks at the beginning of the outbreak in 2004; culling reduced that number to <1 million by August 2005.

eed of Muscovy ducks and native ducks). If a single case of H5N1 infection is detected in a village, all the poultry in the village are culled. Approximately 1.0 million to 1.5 million ducks were raised as backyard ducks at the beginning of the outbreak in 2004; culling reduced that number to <1 million by August 2005. National Surveillance Program In response to the H5N1 influenza outbreaks in 2004, the government of Thailand dispatched teams to villages to identify infected birds and cull flocks in which infection was detected.

eed of Muscovy ducks and native ducks). If a single case of H5N1 infection is detected in a village, all the poultry in the village are culled. Approximately 1.0 million to 1.5 million ducks were raised as backyard ducks at the beginning of the outbreak in 2004; culling reduced that number to <1 million by August 2005. National Surveillance Program In response to the H5N1 influenza outbreaks in 2004, the government of Thailand dispatched teams to villages to identify infected birds and cull flocks in which infection was detected. Sample Collection, Histopathology, Virus Isolation, and Serology During the study period (February to September 2004), our laboratory received 450 sick, moribund, or dead ducks from 25 flocks in the western and central provinces of Thailand. In the detailed studies (Table 1), blood was sampled for serologic analysis by the hemagglutination inhibition (HI) test. All moribund ducks were euthanized, and their internal organs were collected, fixed with 10% buffered formalin, and processed for histopathologic analysis. Additionally, parts of the brain, lung, trachea, intestine, liver, pancreas, kidney, ovary, oviduct, testes, heart, and tight muscle were collected for virus isolation. The tissues were ground and filtered through 0.2–μ filters. The filtrates of each organ were injected into 9- to 11-day-old embryonated chicken eggs and incubated at 37°C for 2 days. The eggs were observed daily to determine whether death occurred. The allantoic fluid was harvested and tested for influenza virus by HI assay. Any positive sample was then subtyped for H5N1. A second egg passage was performed if the embryonated eggs were still alive 72 hours after injection.

ubated at 37°C for 2 days. The eggs were observed daily to determine whether death occurred. The allantoic fluid was harvested and tested for influenza virus by HI assay. Any positive sample was then subtyped for H5N1. A second egg passage was performed if the embryonated eggs were still alive 72 hours after injection. Table 1 Studies of H5N1 influenza in grazing ducks in Thailand, February to July 2004* Flock no. Approximate no. ducks Age when positive for H5N1 virus (d) Duration of virus shedding before detection of illness or culling (d) Highest viral titer (log10 EID50/mL) Antibody titers to H5N1 (HI) (log2) before culling 1† 4,600 66 8 2.0 <1‡ 2§ 5,200 78 10 3.1 2 3† 8,000 42 5 2.0 <1 4† 6,800 74 7 2.5 2 5† 4,300 93 5 3.3 2 6¶ 7,200 59 5 3.6 2 7¶ 10,000 82 7 ND ND 8† 6,300 60 9 3.8 2 9† 9,800 71 10 ND ND 10† 5.500 51 6 3.4 ND *EID50, 50% egg infectious dose; HI, hemagglutination inhibition; ND, not done. †Suphanburi Province. ‡Serum samples collected ≈12 d after flock moved to rice field. §Nakornpathom Province. ¶Ayuthdhaya Province. H5N1 Subtyping Avian influenza virus was subtyped by HI assay by using antiserum specific against the H5 hemagglutinin. Reverse-transcription polymerase chain reaction (RT-PCR) analysis was used for H5 and N1 typing (14). Immunohistochemical Testing To evaluate histologic changes, we used immunohistochemical testing by indirect immunoperoxidase staining as described (15). Tissue was fixed in formalin before being embedded in paraffin, then cut in 5–μ-thick sections and mounted onto silanized slides.

H5N1 Subtyping Avian influenza virus was subtyped by HI assay by using antiserum specific against the H5 hemagglutinin. Reverse-transcription polymerase chain reaction (RT-PCR) analysis was used for H5 and N1 typing (14). Immunohistochemical Testing To evaluate histologic changes, we used immunohistochemical testing by indirect immunoperoxidase staining as described (15). Tissue was fixed in formalin before being embedded in paraffin, then cut in 5–μ-thick sections and mounted onto silanized slides. Criteria for Culling Ducks The criteria for culling duck flocks were based on H5N1 virus isolation and identification by serologic and RT-PCR analysis (12). During the screening of village poultry in 2004, a single positive virus isolation resulted in the culling of all poultry (e.g., chicken, ducks, geese, quail) in the entire village. If serologic evidence of infection was detected, cloacal swabs of 60 ducks in that flock were collected and processed for virus isolation in embryonated chicken eggs. Results Detection of Influenza Viruses in Different Duck-raising Systems Closed High-Biosecurity System As mentioned earlier, ≈1% of every duck flock was sampled for H5N1 detection before being sent to slaughter. More than 10,000 ducks were tested during the study period. No virologic or serologic evidence of H5N1 virus infection was detected in the birds raised in this closed system in western Thailand, including Nakornpathom and Kanchanaburi provinces, despite cocirculation of H5N1 influenza viruses in other duck-raising systems in the region.

ucks were tested during the study period. No virologic or serologic evidence of H5N1 virus infection was detected in the birds raised in this closed system in western Thailand, including Nakornpathom and Kanchanaburi provinces, despite cocirculation of H5N1 influenza viruses in other duck-raising systems in the region. Open House System Most farms that raised ducks with the open house system are in western Thailand, including the 4 provinces of Nakornpathom, Kanchanaburi, Suphanburi, and Rachaburi. Birds from 17 farms were tested for infection with virus; in birds from 4 (23.5%), infection with the H5N1 virus was detected.

ucks were tested during the study period. No virologic or serologic evidence of H5N1 virus infection was detected in the birds raised in this closed system in western Thailand, including Nakornpathom and Kanchanaburi provinces, despite cocirculation of H5N1 influenza viruses in other duck-raising systems in the region. Open House System Most farms that raised ducks with the open house system are in western Thailand, including the 4 provinces of Nakornpathom, Kanchanaburi, Suphanburi, and Rachaburi. Birds from 17 farms were tested for infection with virus; in birds from 4 (23.5%), infection with the H5N1 virus was detected. Grazing System In 28 (45.9%) of the 61 free-range duck flocks tested, infection with H5N1 influenza virus was detected. Investigators studied H5N1 infection in 10 flocks of grazing ducks in Ayuthdhaya, Nakornpathom, and Suphanburi provinces between February and July 2004 to determine the biologic and pathologic features of H5N1 infection in the field (Table 1). No virologic or serologic evidence of H5N1 infection was detected in any of the flocks while they were located in the brooding houses. However, after they were moved outdoors to the rice fields, infection with H5N1 influenza was detected in all 10 flocks; the earliest infection was detected 12 days after the ducks left the brooding houses (flock 3, at 42 days of age). The interval between leaving the brooding houses and detection of H5N1 infection was 12–63 days. Of the 10 flocks, 3 (flocks 2, 8, and 9) showed disease signs; only a few birds (<1%) in each flock were clinically affected. However, the interval between initial detection of H5N1 viruses in the flock and culling was 5–10 days, which supports the contention that most ducks in the flocks showed no disease signs.

days. Of the 10 flocks, 3 (flocks 2, 8, and 9) showed disease signs; only a few birds (<1%) in each flock were clinically affected. However, the interval between initial detection of H5N1 viruses in the flock and culling was 5–10 days, which supports the contention that most ducks in the flocks showed no disease signs. Serologic evaluation of the flocks showed that low titers of HI antibody were detected before culling, which indicates that an immune response had already begun without disease signs in most birds. Cloacal virus titers in individual ducks showing disease signs before culling were 2.0–3.8 log10 50% egg infectious dose (EID)50/mL which shows that virus was being shed in feces (Table 1). Similar virus titers were detected in asymptomatic ducks. Signs of disease in flocks, 2, 8, and 9 were depression, lethargy, cloudy cornea, and blindness. However, no deaths were observed in the 10 days before culling. Backyard Ducks Of the backyard poultry, chickens were the most frequently infected; 56% of the chicken flocks tested were positive for H5N1 influenza (12). Ducks were the second most frequently infected; 27% of backyard duck flocks were positive for H5N1. During the second wave of H5N1 infection of poultry and humans in Thailand (August–November 2004), 47% of backyard duck flocks were H5N1 positive. During this time, scientists realized that most ducks infected with H5N1 were asymptomatic.

ond most frequently infected; 27% of backyard duck flocks were positive for H5N1. During the second wave of H5N1 infection of poultry and humans in Thailand (August–November 2004), 47% of backyard duck flocks were H5N1 positive. During this time, scientists realized that most ducks infected with H5N1 were asymptomatic. Pathologic Features As previously mentioned, our laboratory received 450 sick, moribund, or dead ducks, which were studied for pathologic features of H5N1 infection. These birds had been raised in the open house system or were from backyard flocks. They exhibited signs of disease such as high fever, dyspnea, depression, and diarrhea, and nervous signs such as ataxia, incoordination, and convulsions (Figure 3A). Most had ocular and nasal discharge accompanied by conjunctivitis; 20%–100% of the birds in each flock from which these ducks originated were dead. All cloacal and tracheal swabs and tissue samples were positive for H5N1 by HI and RT-PCR (results not shown). Figure 3 A) A White Cherry Valley duck (Anas platyrhynchos), infected with HPAI H5N1 displays nervous signs, convulsions. B) Histopathologic features of the lung of an HPAI H5N1–infected white Cherry Valley duck; infiltration of inflammatory cells in the lung parenchyma (magnification ×100).

Pathologic Features As previously mentioned, our laboratory received 450 sick, moribund, or dead ducks, which were studied for pathologic features of H5N1 infection. These birds had been raised in the open house system or were from backyard flocks. They exhibited signs of disease such as high fever, dyspnea, depression, and diarrhea, and nervous signs such as ataxia, incoordination, and convulsions (Figure 3A). Most had ocular and nasal discharge accompanied by conjunctivitis; 20%–100% of the birds in each flock from which these ducks originated were dead. All cloacal and tracheal swabs and tissue samples were positive for H5N1 by HI and RT-PCR (results not shown). Figure 3 A) A White Cherry Valley duck (Anas platyrhynchos), infected with HPAI H5N1 displays nervous signs, convulsions. B) Histopathologic features of the lung of an HPAI H5N1–infected white Cherry Valley duck; infiltration of inflammatory cells in the lung parenchyma (magnification ×100). At necropsy, gross lesions were detected, including ecchymotic or petechial hemorrhage of leg and footpad; serous fluid surrounding the heart, pancreas, liver, and abdomen; cyanosis of the oral cavity; and mild pleural effusion. On histopathologic examination, the most striking lesions were found in the lung, with extensive pneumonia and severe pulmonary edema with hyaline material in the alveolar space and slight mononuclear infiltration in the area surrounding congested vessels (Figure 3B). Nonsuppurative encephalitis with perivascular cuffing of mononuclear cells and gliosis were detected in the brains of ducks that displayed nervous signs. Hyaline degeneration and necrosis of myocardium with mononuclear infiltration were detected predominantly in dead ducks from fast-growing breeds such as the Pekin and white Cherry Valley ducks. Necrotizing pancreatis with mononuclear infiltration was detected in all affected ducks. Most affected ducks exhibited focal hepatitis, tubulonephritis, splenic lymphoid depletion or necrosis, and enteritis. Virus antigen was detected by immunohistochemical tests in all organs tested, including trachea, lung, liver, pancreas, rectum, bursa of Fabricius, spleen, brain, heart, and kidney (Figure 4).

d ducks. Most affected ducks exhibited focal hepatitis, tubulonephritis, splenic lymphoid depletion or necrosis, and enteritis. Virus antigen was detected by immunohistochemical tests in all organs tested, including trachea, lung, liver, pancreas, rectum, bursa of Fabricius, spleen, brain, heart, and kidney (Figure 4). Figure 4 Immunohistochemistry of an HPAI H5N1–infected white Cherry Valley duck (Anas platyrhynchos). The viral antigen is detected in myocardial cells and lymphoid cells (arrow) (A) and renal tubular cells (B) (magnification ×100). The primary antibody used for immunohistochemistry in this study was a mouse anti–avian influenza H5 antibody (Magellan Biotechnology, Chunan, Taiwan).

rry Valley duck (Anas platyrhynchos). The viral antigen is detected in myocardial cells and lymphoid cells (arrow) (A) and renal tubular cells (B) (magnification ×100). The primary antibody used for immunohistochemistry in this study was a mouse anti–avian influenza H5 antibody (Magellan Biotechnology, Chunan, Taiwan). Experimental Infection of Khaki Campbell Ducks Because culling of all H5N1–positive ducks was mandated in Thailand, we could not determine the natural outcome of infection in birds raised in the open on rice fields. Therefore, khaki Campbell ducks were experimentally infected with 4 representative H5N1 viruses isolated in Thailand in 2004 and 2005. All animal experiments were performed in biosafety level 3+ facilities. All 4 viruses caused the deaths of infected ducks; however, their degree of death varied (Table 2). The most lethal virus tested was A/duck/Thailand/71.1/2004, which caused death in 10/10 of the infected khaki Campbell ducks, a lethality rate comparable to that previously reported for Mallard ducks (16). Also tested was a human virus isolated in 2004, A/Thailand/MK2/2004, which resulted in the death of 2/10 khaki Campbell ducks. Of the two 2005 viruses tested, 1 caused very slight disease and resulted in only 1/10 deaths (A/quail/Thailand/551/2005) whereas the other (A/duck/Thailand/144/2005) resulted in 5/10 deaths. Ducks inoculated with A/Thailand/MK2/04 shed virus for the longest period of time (day 10 postinfection), whereas the 2005 virus isolates were shed only until day 8 postinfection. These results indicate that the H5N1 avian viruses recently isolated in Thailand can cause death in khaki Campbell ducks; however, several infected ducks remained completely healthy with no signs of disease throughout the study.

0 postinfection), whereas the 2005 virus isolates were shed only until day 8 postinfection. These results indicate that the H5N1 avian viruses recently isolated in Thailand can cause death in khaki Campbell ducks; however, several infected ducks remained completely healthy with no signs of disease throughout the study. Table 2 Experimental infection of khaki Campbell ducks with viruses isolated in Thailand, 2004–2005 Virus* Deaths† Illness† Day detectable virus was shed‡ 2 4 6 8 10 A/duck/Thailand/144/05 5/10 3/10 10/10 9/9 1/5 0/5 0/5 A/quail/Thailand/551/05 1/10 2/10 8/10 8/10 1/9 0/9 0/9 A/Thailand/MK2/04 2/10 2/10 9/10 10/10 6/8 2/8 2/8 A/duck/Thailand/71.1/04 10/10 10/10 10/10 1/1 –§ – – *Eight 4-week-old khaki Campbell ducks were injected with 106 50% egg infectious dose of virus by intranasal and intratracheal infection, and 2 contact ducks were introduced 1 day later. †Total number of deaths or birds showing disease/total number of birds. Birds were observed daily for signs of disease or death. ‡Number of ducks shedding by the trachea or cloacae/total number of ducks remaining alive. Ducks were swabbed every other day beginning on day 2 postinfection. §All of the ducks in this group died.

number of deaths or birds showing disease/total number of birds. Birds were observed daily for signs of disease or death. ‡Number of ducks shedding by the trachea or cloacae/total number of ducks remaining alive. Ducks were swabbed every other day beginning on day 2 postinfection. §All of the ducks in this group died. Current Status of Duck Raising in Thailand As of October 2005, the government of Thailand forbids the practice of raising ducks in open fields and moving grazing ducks from 1 region to another. Farmers who do so are subject to fines and other punishments. Additionally, they receive no compensation if they raise ducks in the open free-range system, and the ducks become infected with H5N1. Farmers were initially compensated for the culling of their ducks. Duck raising is now confined to the high-biosecurity system.

ers who do so are subject to fines and other punishments. Additionally, they receive no compensation if they raise ducks in the open free-range system, and the ducks become infected with H5N1. Farmers were initially compensated for the culling of their ducks. Duck raising is now confined to the high-biosecurity system. After a lull of almost 1 year, a case of human H5N1 infection was reported in Thailand in October 2005. The report was preceded by the illegal grazing of 3 flocks of 3,000 to 5,000 free-range ducks in rice fields in the area (Kanchanaburi Province). Although no direct contact between the grazing ducks and backyard chickens was known, within 2 weeks of the arrival of the ducks, chickens in the area began dying, and a person who had direct contact with the diseased chickens died of H5N1 infection. Approximately 500 backyard chickens were culled in the village. Sequence analysis of the human isolate and avian isolates (duck and chicken) from this area would be essential to confirm the epidemiologic link between these cases and, coupled with the chronology of events, to assess whether free-grazing ducks were indeed the source of infection for this outbreak.

led in the village. Sequence analysis of the human isolate and avian isolates (duck and chicken) from this area would be essential to confirm the epidemiologic link between these cases and, coupled with the chronology of events, to assess whether free-grazing ducks were indeed the source of infection for this outbreak. Discussion The 4 duck-raising systems in wide use at the beginning of the 2004 Thai epidemic differed markedly in cases of influenza detected. No infections with H5N1 influenza virus were detected in ducks raised in the closed system, attesting to the effectiveness of the biosecurity employed. In contrast, H5N1 infection was detected in ducks raised in all 3 open systems. Notably, infection in the hatchery or during the 3 weeks of brooding was detected only after the ducks were released into the rice fields. The source of the H5N1 viruses infecting domestic ducks in the rice fields remains controversial. Because H5N1 viruses were detected in herons, storks, egrets, and other dead waterfowl in Eastern Asia, the initial spread of the highly pathogenic viruses in this region of the world has been attributed to wild migrating birds. What role wild migrating birds had in the spread of H5N1 influenza virus is now a moot question. The widespread outbreaks and massive die-off of bar-headed geese and other species in western China (17,18), and the spread of H5N1 to central Asia (Kazakhstan, southern Russia, and Turkey) and more recently to Romania and Croatia in eastern Europe, are likely caused by wild migratory birds.

rus is now a moot question. The widespread outbreaks and massive die-off of bar-headed geese and other species in western China (17,18), and the spread of H5N1 to central Asia (Kazakhstan, southern Russia, and Turkey) and more recently to Romania and Croatia in eastern Europe, are likely caused by wild migratory birds. Detailed studies of 10 flocks of grazing ducks in Thailand in the present study showed infection with H5N1 influenza virus in all flocks. Although the ducks shed virus for 5 to 10 days, few ducks showed disease signs, and in some flocks, no ducks were symptomatic. Prolonged shedding of H5N1 viruses in experimentally infected ducks has been previously described (16,19), but prolonged shedding in free-range ducks has not. Therefore, free-range (grazing) ducks that are moved long distances by truck and that do not necessarily show disease signs are an optimal vehicle for the spread of H5N1 viruses throughout the country. These findings support the need for regulations that forbid the practice of raising ducks on the free range, a need underscored by the association of the recent human infection with illegal free-range duck grazing.

essarily show disease signs are an optimal vehicle for the spread of H5N1 viruses throughout the country. These findings support the need for regulations that forbid the practice of raising ducks on the free range, a need underscored by the association of the recent human infection with illegal free-range duck grazing. This study also points out the dangers of raising ducks in the open systems without complete biosecurity. Although stopping the commercial raising of ducks in open system may be impossible, the more problematic issue is that of backyard ducks, which are part of traditional village livestock. Highly pathogenic H5N1 influenza virus is now likely endemic in poultry in Vietnam, Cambodia, China, and Indonesia. The vaccine option should be considered if backyard duck raising is to continue in Southeast Asia.

e, the more problematic issue is that of backyard ducks, which are part of traditional village livestock. Highly pathogenic H5N1 influenza virus is now likely endemic in poultry in Vietnam, Cambodia, China, and Indonesia. The vaccine option should be considered if backyard duck raising is to continue in Southeast Asia. Although no human cases of H5N1 have been attributed to direct contact with ducks in Thailand, free-grazing ducks have been identified as a risk factor for the occurrence of H5N1 outbreaks among chickens (13). In Vietnam, however, reported human cases of H5N1 influenza have potentially been linked to the consumption of raw duck blood dishes (http://www.who.int/csr/don/2005_01_21/en/index.html). Therefore, H5N1-infected ducks are a risk factor for both commercial and backyard poultry and potentially for humans as well. Since the introduction of the nationwide comprehensive surveillance program ("x-ray surveys") in Thailand (12) and the culling of all infected poultry, human cases of H5N1 infection have been markedly reduced. Traditional methods of duck raising in Thailand and in the rest of Southeast Asia must be modified if we are to control highly pathogenic H5N1 avian influenza. Suggested citation for this article: Songserm T, Jun-on R, Sae-Heng N, Meemak N, Hulse-Post DJ, Sturm-Ramirez KM,‡ et al. Domestic ducks and H5N1 influenza epidemic, Thailand. Emerg Infect Dis [serial on the Internet]. 2006 Apr [date cited]. http://dx.doi.org/10.3201/eid1204.051614

Although no human cases of H5N1 have been attributed to direct contact with ducks in Thailand, free-grazing ducks have been identified as a risk factor for the occurrence of H5N1 outbreaks among chickens (13). In Vietnam, however, reported human cases of H5N1 influenza have potentially been linked to the consumption of raw duck blood dishes (http://www.who.int/csr/don/2005_01_21/en/index.html). Therefore, H5N1-infected ducks are a risk factor for both commercial and backyard poultry and potentially for humans as well. Since the introduction of the nationwide comprehensive surveillance program ("x-ray surveys") in Thailand (12) and the culling of all infected poultry, human cases of H5N1 infection have been markedly reduced. Traditional methods of duck raising in Thailand and in the rest of Southeast Asia must be modified if we are to control highly pathogenic H5N1 avian influenza. Suggested citation for this article: Songserm T, Jun-on R, Sae-Heng N, Meemak N, Hulse-Post DJ, Sturm-Ramirez KM,‡ et al. Domestic ducks and H5N1 influenza epidemic, Thailand. Emerg Infect Dis [serial on the Internet]. 2006 Apr [date cited]. http://dx.doi.org/10.3201/eid1204.051614 Acknowledgments We thank Carol Walsh and Amanda Ball for manuscript preparation and Margaret Carbaugh for editing the manuscript.

Suggested citation for this article: Songserm T, Jun-on R, Sae-Heng N, Meemak N, Hulse-Post DJ, Sturm-Ramirez KM,‡ et al. Domestic ducks and H5N1 influenza epidemic, Thailand. Emerg Infect Dis [serial on the Internet]. 2006 Apr [date cited]. http://dx.doi.org/10.3201/eid1204.051614 Acknowledgments We thank Carol Walsh and Amanda Ball for manuscript preparation and Margaret Carbaugh for editing the manuscript. Support for Thaweesak Songerm, Rungroj Jun-on, Namdee Sae-Heng, and Noppadol Meemak was provided by Kasetsart University Research and Development Institute, Thailand. Support for Robert G. Webster, Diane Hulse-Post, and Katharine M. Sturm-Ramirez was provided by US Public Health Service grant AI95357 and by the American Lebanese Syrian Associated Charities. Dr Songserm is a veterinary pathologist in the Faculty of Veterinary Medicine, Kasetsart University, Kamphaengsaen Campus, Nakornpathom, Thailand. His research interests include avian pathology, diseases of ducks and geese, and emerging diseases in animals.

Jenny Hammond, The Natural History of Influenza A Viruses (1990). Stained Glass, 21 in × 56 in / 53.3 cm × 142.2 cm. Commissioned by Robert and Marjorie Webster, Memphis, TN, USA. Digital image courtesy of Robert Webster. On a rainy and misty day in late 1989, my wife (Marjorie) and I were walking the path along the remnants of Hadrian’s Wall, a UNESCO world heritage site near the border between England and Scotland. The Romans began building this wall—which extends from the banks of the river Tyne on the west coast to Solvay Firth on the east coast of England—ostensibly to keep the “barbarian” Scots from plundering their English territory. During lunch in a local pub, we discovered in a local publication a picture of a wonderful stained glass window depicting a dragon. We arranged to visit the artist, Jenny Hammond, at her nearby farm in Highgreenleycleugh, Northumberland, England, where we viewed her stained glass works firsthand and commissioned her to create a unique stained glass window that would detail the natural history of influenza. After we returned to our home in Memphis, Tennessee, we sent Hammond several review articles and electron micrographs to provide her some background on influenza A viruses. Hammond, in turn, shared her ideas through penciled sketches and over the next year completed the version that appears on this month’s EID journal cover (Figure).

ed to our home in Memphis, Tennessee, we sent Hammond several review articles and electron micrographs to provide her some background on influenza A viruses. Hammond, in turn, shared her ideas through penciled sketches and over the next year completed the version that appears on this month’s EID journal cover (Figure). Figure A different perspective of this stained glass window has also appeared on the cover of the book Microbial Threats to Health: Emergence, Detection, and Response (2003), by the Committee on Emerging Microbial Threats to Health in the 21st Century, Board on Global Health, Institute of Medicine, National Academies Press; another appears on the cover of a series of workshop summaries also published by the Institute of Medicine, National Academies Press. After its transport by air, Marjorie and I installed the stained glass window into the premeasured window frame near the front door of our home. Visiting students and colleagues from around the world invariably ask to photograph the window. This stained glass window offers viewers a concise introduction to influenza in a One Health system in which viruses emerge from wild bird reservoirs and periodically cause pandemic diseases (such as influenza) in humans.

e. Visiting students and colleagues from around the world invariably ask to photograph the window. This stained glass window offers viewers a concise introduction to influenza in a One Health system in which viruses emerge from wild bird reservoirs and periodically cause pandemic diseases (such as influenza) in humans. Although the term “One Health” was recently coined, it describes an ancient concept recognized by Hippocrates in his text “On Airs, Waters, and Places.” Scientists have noted the similarity in disease processes between animals and humans since the 1800s. Rudolf Virchow, a 19th century German pathologist and anthropologist, devised the term “zoonosis” to indicate web of the infectious diseases links between animals and humans, saying that “... between animal and human medicine there are no dividing lines—nor should there be.” In the 20th century, the One Health concept coalesced and gained momentum in the public health and animal health communities. The work of art depicted on this month’s cover depicts that interrelationship of human, animal, and environmental health.

mal and human medicine there are no dividing lines—nor should there be.” In the 20th century, the One Health concept coalesced and gained momentum in the public health and animal health communities. The work of art depicted on this month’s cover depicts that interrelationship of human, animal, and environmental health. The dark blue glass prominently positioned in the upper right signifies the global problem of influenza A viruses, which are associated with yearly epidemics and intermittent pandemics. The came strips, which provide structure for the window, also depict the spread of virus, which has a large reservoir and vast gene pool in wild migratory aquatic birds—including ducks and gulls represented in the window as well as shorebirds, geese, and terns. The influenza viruses can spread to pigs, considered the intermediate host, and to humans. The red background depicts the high fever in pigs and humans infected with the influenza virus. Hammond also incorporated microscopic details essential to natural history of influenza A. Her depiction of the influenza virus particles show the spiky surface made up of the hemagglutinin that attaches the virus to the respiratory tract of the host and the neuraminidase that releases the virus from infected cells so that the virus can spread. She has depicted the RNA genome of 8 segments as separate threads. The particles with multiple threads illustrate how reassortment between influenza viruses gives rise to new pandemic strains.

e respiratory tract of the host and the neuraminidase that releases the virus from infected cells so that the virus can spread. She has depicted the RNA genome of 8 segments as separate threads. The particles with multiple threads illustrate how reassortment between influenza viruses gives rise to new pandemic strains. Stained-glass windows have been appreciated for their utility and splendor for more than 1,000 years, and this engaging work of art reminds us that influenza A viruses—which can be easily spread between animals and human, use various host species, and exist in many different environments—remain an enduring and global health concern. Suggested citation for this article: Webster RG. Illustrating the natural history of influenza A viruses through art. Emerg Infect Dis. 2016 Dec [date cited]. http://dx.doi.org/10.3201/eid2212.AC2212