BAOJ Veterinary Science - Bio Accent

BAOJ Veterinary Science Atul Kumar, BAOJ Vet Sci, 2018, 2: 1 2: 005

Review

Zoonoses at the Human-Avian Interface: A Review Atul Kumar1*, Devina Sharma2 and Rakesh Kumar3 Department of Veterinary Public Health and Epidemiology, DGCN COVAS, CSK Himachal Pradesh Agricultural University, Palampur (India) – 176062

1

Department of Veterinary Parasitology, DGCN COVAS, CSK Himachal Pradesh Agricultural University, Palampur (India) – 176062

2

Department of Veterinary Pathology, DGCN COVAS, CSK Himachal Pradesh Agricultural University, Palampur (India) – 176062

3

Abstract Birds, a significant member of our ecosystem are also a major reservoir for many zoonotic infections. They can transmit several emerging and reemerging infectious diseases to humans mostly through direct contact or consumption of contaminated meat, eggs, and water. With the ever-growing expansion of global trade, population explosion, human movement and changing demographic behavior, there has been tremendous eversion of pathogens. Such infections continue to pose risks to human health in most parts of world and are economically important too. This review, focused on the most important infectious diseases of poultry which can cause human health hazard by describing general information, epidemiology, clinical signs, and strategies for prevention/control with the objective to create awareness among all the stakeholders to avoid associated fatal complications.

Keywords: Poultry; Zoonoses; Epidemiology; Human Health

with or being around live birds and secondly, through consumption of contaminated chicken and eggs from the infected birds. The occurrence of zoonoses depends on a number of factors such as: duration of exposure, effective contact, pathogenicity and virulence of the pathogen and its survival, route of infection and transmission, involvement of mechanical and biological vectors, etc. Zoonotic diseases in poultry exert dual impacts on human population. This could be either through direct risk of infection or through reduced production by the birds resulting in food insecurity and poverty [2]. Human health problems resulting from direct or indirect contact with live infected birds and their secretions, excretion or food products are associated with bacterial, viral, fungal and chlamydial agents (Table 1). The present review describes such infectious diseases/ agents of avian species which can pose serious risks/threats to human health as well as recent information on their prevalence and epidemiological observations reported from various geographical regions of world including India (Table 2).

Introduction Livestock rearing is one of the most important economic activities in the rural areas of most of the developing regions of world. It not only acts a source of income to most of the families dependent on agriculture but is also a source of protein supplement to the family members of the household in the form of milk, meat and eggs. Therefore, animal husbandry acts as adjunct to agriculture and it is crucial for overall food security too. In the livestock sector, poultry industry is considered to be the fastest growing industry among the agriculture based industries. With the growing popularity of backyard and small production flocks, the concerns regarding human health risks associated with poultry diseases are also increasing. There are various diseases/infections that are naturally transmissible between vertebrate animals and man, commonly referred to as zoonoses [1]. In general, humans can get infection from poultry through contact

BAOJ Vet Sci, an open access journal

*Corresponding Author: Atul Kumar, Assistant Professor, Department of Veterinary Public Health and Epidemiology, Dr. G. C. Negi College of Veterinary and Animal Sciences, CSK Himachal Pradesh Agricultural University, Palampur (India) – 176062, Tel No: +91 9481002944; E-mail: [email protected] Sub Date: March 30th, 2018, Acc Date: April 23th, 2018, Pub Date: April 24th, 2018. Citation: Atul Kumar, Devina Sharma and Rakesh Kumar (2018) Zoonoses at the Human-Avian Interface: A Review. BAOJ Vet Sci 2: 005. Copyright: © 2018 Atul Kumar. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Volume 2; Issue 1; 005

Citation: Atul Kumar, Devina Sharma and Rakesh Kumar (2018) Zoonoses at the Human-Avian Interface: A Review. BAOJ Vet Sci 2: 005.

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Table 1: The zoonotic agent associated with birds and their transmission dynamics Agents

Diseases/Infections

Major mode of transmission of infection from infected birds to humans

Viruses

Avian Influenza

Contact with live infected birds and their secretions and excretions

West Nile Virus infection

Bites from infected mosquitoes

New Castle Disease

Contact with live infected birds and their secretions and excretions

Campylobacteriosis

Contaminated meat and water

Colibacillosis

Contaminated poultry meat, eggs and water

Salmonellosis

Contaminated poultry meat, eggs and water

Avian Tuberculosis

Direct contact with infected birds, ingestion of contaminated feed and water, or contact with a contaminated fomites.

Protozoan

Toxoplasmosis

Contaminated poultry meat

Fungi

Aspergillosis

Inhalation of spores present in soil, water and feed

Cryptococcosis

Inhaling dust contaminated with bird droppings

Histoplasmosis

Contact with soil contaminated by bird or bat droppings

Ornithosis

Inhalation of organism shed by infected birds, handing of dead infected birds, nasal discharge, bite and person to person contact

Bacteria

Chlamydia

Table 2: Avian Zoonoses: Recent trends, epidemiological features and reports Disease

Spatial distribution (Host)

Avian Influenza

India (Poultry)

H5N1 outbreak occurred resulting in mortality of 1760 birds and culling of 5,263 birds

2016

[109]

India (Poultry)

Highly pathogenic avian influenza (H5N8) viruses detected in waterfowls. Both viruses were different 7:1 reassortmants of H5N8 viruses isolated from wild birds in the Russian Federation and China, suggesting virus spread during southward winter migration of birds.

2017

[110]

Global occurrence (Human)

A total of 860 human cases of avian influenza A(H5N1) have been reported from 16 countries globally with 454 deaths.

2017

[111]


Major epidemiological observations

Year of report

Reference



West Nile Disease

New Castle Disease

Campylobacteriosis

Colibacillosis

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India (Poultry)

H5N8 reported with 9 cases and 942 slaughtered

2018

[112]

China (Human)

A total of 1557 laboratory-confirmed human infections with avian influenza A(H7N9) virus reported since early 2013.

2018

[113]

India (Birds)

2.46% of birds showed evidence of flavivirus antibodies suggesting rare infection among wild migratory birds

2012

[114]

India (Ducks)

WNV specific antibodies detected in 11.5% of duck in Kerala, India.

2016

[115]

India (Humans)

Neutralizing antibodies against WNV was found in 21.5% of tested human sera

2017

[116]

India (Mosquitoes and Poultry)

WNV identified from field-collected Culex pseudovishnui and Mansonia uniformis. The study also highlighted the role of sentinel chickens for WNV surveillance.

2017

[117]

United Kingdom (Human)

New Castle Disease virus as a cause of human conjunctivitis due to exposure to large quantities of virus.

2000

[118]

United States of America (Human)

Mild, self-limiting influenza like disease with fever and headache reported in humans

2003

[119]

United States of America (Human)

Isolation and identification of avian paramyxovirus 1 (APMV-1) from a lethal 2007 case of human pneumonia.

[120]

US (Poultry)

Crop of poultry is an important niche for Campylobacter and may represent a 2015 major source of contamination during processing.

[121]

India (Poultry and Human)

C. jejuniwere more frequent than C. coli in poultry and chicken acts as a potential source of infection to children

2013

[122]

Switzerland (Poultry and Human)

Prevalence of Campylobacter in broilers, with a 2-week lag, has a significant impact on disease incidence in humans

2015

[123]

USA (Poultry and Human)

Multistate outbreak of campylobacteriosis associated with consumption of undercooked chicken liver

2015

[124]

Brazil (Poultry)

Avian pathogenic E. coli (APEC) is a reservoir/subpathotype of human Extraintestinal Pathogenic E. coli (ExPEC)

2017

[125]

USA (Poultry, rats and humans)

E. coliisolates from healthy chicken feces contain ExPEC-associated genes, exhibit ExPEC-associated in vitro phenotypes, and can cause ExPECassociated infections in animal models, and thus may pose a health threat to poultry and consumers.

2017

[126]

India (Poultry)

Colibacillosis in poultry with prevalence of 17.16% and highest prevalence at the age group of 3-6 weeks in Assam (India).

2018

[127]




Salmonellosis

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Republic of Srpska (Poultry)

Higher incidence of Multidrug-resistant Salmonella Infantis in poultry meat than S. Enteritidis

2017

[128]

India (Poultry)

Isoaltion of S. Enteritidis, S.Typhimurium in addition to S. Gallinarum from Fowl typhoid affected birds in winters.

2015

[129]

India (Poultry)

Poultry litter, environmental and post evisceration stages at retail chicken processing, are critical sources of cross contamination of invasive Salmonella spp.

2017

[130]

Japan (Human)

Dry pleurisy complicating solitary pulmonary nodules in humans caused by Mycobacterium avium

2015

[131]

Republic of Korea (Humans)

Hydropneumothorax in lung diseases of humans caused by M. avium and M. intracellulare

2016

[132]

India (Poultry)

The prevalence of Toxoplasma antibodies in chicken was found to be 18.7%

2005

[133]

China (Poultry)

The prevalence of Toxoplasma antibodies in chicken was found to be 67.14% 2017 from farms with T. gondii positive in soil and 41.0% from farms with T. gondii negative in soil.

[134]

Kenya (Poultry)

Brain samples of chicken revealed overall T. gondii prevalence of 79.0%

2016

[135]

Italy (Poultry)

Chicken Meat juice serology revealed 36.4% prevalence of T. gondiiantibodies 2016

[136]

Brazil (Poultry)

Four new genotypes of T. gondii were described with 16.6% seroprevalence.

2018

[137]

Aspergillosis

Kalyoubia Governorate, (Human)

A. fumigatusisolated from sputum samples of poultry farm workers.

2014

[138]

Cryptococcosis

Thailand (Human)

Cryptococcal meningitis in HIV affected patients.

2004

[139]

Histoplasmosis

Bangladesh (Human)

Ulcers in nasopharynx and granulomatous lymphadenitis in patients affected with HIV who contracted the infection from soil infected with bird’s droppings.

2010

[140]

West Africa (Human)

A total of 470 cases of Histoplasmosis have been reported since 1952-2017. The majority of cases were found to be caused by H. capsulatum.

2018

[141]

Hong Kong (Human)

Human beings in close contact with birds acquired the respiratory infection indicated Chlamydial infection.

2015

[142]

New south Wales (Human)

Nine people developed the respiratory illness due to exposure to fetal membranes of a mare.

2017

[143]

Avium Tuberculosis

Toxoplasmosis

Chlamydiosis




Viral Agents Transmissible from Poultry to Humans Viral infections are the most common cause of losses, not only in large commercial flocks, but also in backyard poultry. Most viral diseases in poultry do not respond to drug treatment. Therefore, treatment is either not recommended or relies on supportive therapy. The prevention and control strategies are cornerstone in limiting economic losses as well restricting the potential risks to human health. This relies on vaccination where this is effective, or by limiting exposure to infected birds. Some common viral zoonotic agents/disease of poultry are:

Avian Influenza Among viral diseases of zoonotic significance, avian influenza is the most dangerous one. In recent past, India suffered multiple outbreaks of avian Influenza (H5N8 and H5N1) at various epicenters in Delhi, Gwalior (MP), Rajpura (Punjab), Hissar (Haryana), Bellary (Karnataka), Allappuzha and Kottayam (Kerala), Ahmedabad (Gujarat), Daman (Daman) and Khordha and Angul [3]. Avian influenza viruses are highly contagious; extremely variable that is widespread in domestic, wild, and ornamental birds. Wild birds in aquatic habitats are thought to be their natural reservoir hosts, but domesticated poultry are readily infected. Influenza viruses belong to the Orthomyxoviridae family. Three types - A, B, and C are distinguished, but the type A viruses are the most important. They can infect both animals and humans. The pathogenicity of influenza viruses results from their significant antigenic variation due to antigenic drift and antigenic shift. As a result, 256 progeny strains can potentially develop [4]. Most viruses cause only mild disease in poultry, and are called low pathogenic avian influenza (LPAI) viruses. Highly pathogenic avian influenza (HPAI) viruses can develop from certain LPAI viruses, usually while they are circulating in poultry flocks [5]. In birds, avian influenza viruses are shed in the feces and respiratory secretions. Fecal-oral transmission is the predominant means of spread in aquatic wild bird reservoirs. Once an avian influenza virus has entered a poultry flock, it can spread on the farm by both the fecal–oral route and aerosols, due to the close proximity of the birds. Fomites can be important in transmission, and flies may act as mechanical vectors [6,7]. Clinical signs in poultry induced by LPAI viruses are some reduction in weight gain in fattening poultry or a slight and temporary decline in egg production in layers [8]. In contrast, HPAI viruses can result in mortalities up to 90-100% in a flock within 48 hours, and cause epidemics that may spread rapidly, devastate the poultry industry and result in severe trade restrictions [9]. Infection of poultry with LPAI viruses capable of evolving into HPAI viruses also affects international trade [10]. Avian influenza is primarily a disease of birds but it may appear among the human population as a result of poor hygiene or prolonged contact with infected birds, their secretions or excretions. The two most commonly reported avian influenza viruses from human clinical cases have been the BAOJ Vet Sci, an open access journal

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Asian lineage H5N1 HPAI viruses, and H7N9 LPAI viruses in China [11]. The people who are at highest risk of getting this infection include poultry farm workers, veterinarians, wildlife biologists, ornithologists etc. Symptoms of avian influenza infection in people are almost similar to common cold and may include fever, malaise, cough, sore throat, muscle aches, abdominal pain, chest pain, conjunctivitis, parenchymal pneumonitis and diarrhoea. However, it may result in much more severe course than classic influenza. For diagnosis, avian influenza viruses can be detected in oropharyngeal, tracheal and/or cloacal swabs from live birds and samples from internal organs of dead birds. In humans, viruses may be found in samples from the upper and/or lower respiratory tract. Viruses can be isolated in embryonated eggs. Real – time polymerase chain reaction (RT-PCR) assays can detect influenza viruses directly in clinical samples, and real – time PCR is the diagnostic method of choice in many laboratories [12]. For screening the flocks, enzyme linked immunoassays including rapid tests are more reliable and quick. Serology may not prove not very useful in diagnosing HPAI infections but is of utmost importance in epidemiological surveillance and demonstrating freedom from infection [13]. There is no specific treatment for influenza virus infections in animals. Poultry flocks infected with HPAI viruses are depopulated (this is generally mandatory in HPAIfree countries). The disposition of infected LPAI flocks may vary with the virus and the country. In humans, treatment for may vary, depending on the severity of the case, and can include various drugs, including antibiotics to treat or prevent secondary bacterial pneumonia, and antivirals. Antiviral drugs are most effective if they are started within the first 48 hours after the onset of clinical signs. Measures to prevent and control cases of zoonotic avian influenza infection include controlling the source of the virus (e.g., closing infected poultry markets); avoiding contact with sick birds, birds known to be infected, and their environments; employing good sanitation and hygiene (e.g., hand washing); and using personal protective equipment (PPE) like respiratory and eye protection such as respirators and goggles, as well as protective clothing including gloves, wherever appropriate. The hands should be washed with soap and water before eating, drinking, smoking, or rubbing the eyes [14]. Since, these viruses have been found in eggs and meat from several avian species, therefore, careful food handling practices are very important when working with poultry or wild game bird products in endemic areas. All poultry products including eggs and meat should be completely cooked before eating [15]. Constant monitoring of avian influenza infections in captive as well as free-living wild birds is part of control programme for avian influenza in India.

West Nile Virus (WNV) West Nile virus (WNV) is an emerging zoonotic arthropod borne flavivirus maintained in mosquito-bird transmission cycle. West Nile virus is



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related to the Japanese and St. Louis encephalitis viruses. It was first isolated from the blood of an ill woman in 1937 in Uganda region of West Nile Delta [16]. In subsequent years, the virus significantly extended its severity, frequency, host range as well as geographical distribution [17,18]. The emergence of WNV in America and its impact on the health of humans, horses and birds, have caused global concern about this virus. West Nile virus causes a potentially fatal encephalomyelitis (inflammation of the brain and spinal cord) in a variety of mammals such as birds, horses, and humans [19, 20]. Birds are natural reservoir hosts and may be clinically or asymptomatically infected. In India, this virus is known to be active in mosquitoes, birds and pigs and there are some reports of its association with human encephalitis cases [21].

been used [24,27]. Specific methods are not available for the treatment of WNV infection. However, in patients with encephalitis supportive therapy is recommended. Though a few candidate vaccines are under laboratory trial, no vaccine has been available commercially for the control of WNV infection in human and animals. The effective prevention and control of human WNV infections depends on the development of comprehensive, integrated mosquito surveillance and control programmes in endemic areas. The integrated mosquito control strategies includes the use of personal protective measures like protective clothing, bed nets, both chemical and plant based mosquito repellants, insecticides, insecticide impregnated curtains, and biological control methods by larvivourus fish, introducing natural parasites and predators and bacterial agents [28,29].

Various species of Culex mosquitoes acts as vectors for WNV. The common species of Culex which have shown competence for both infection and transmission of West Nile virus are Cx. tarsalis and species belonging to Culex pipiens complex. Apart from mosquitoes, the role of other arthropods is also considered in the maintenance of this virus during inter-enzootic periods. The possible role of ardeid birds as vertebrate amplifying host of WNV in the Indian subcontinent was also described by [22]. Though very few clinically overt cases of human encephalitis due to WNV are observed, Japanese encephalitis virus (JEV) is found to dominate in southern India. Infection in humans and horses is most often the result of bites from infected mosquitoes that have fed on infected birds. They are considered as accidental and dead-end hosts. The clinical signs of disease typically present within three to 14 days of exposure. The virus may also be transmitted through contact with other infected birds, their blood, or other tissues. A very small proportion of human to human infections have occurred through organ transplant, blood transfusions and breast milk. Classic clinical signs of horses infected with the WNV include mild to severe ataxia. Signs can range from slight in coordination to recumbency. Some horses exhibit weakness, muscle fasciculation and cranial nerve deficits. Fever is not a consistently recognized feature of the disease in horses [23,24].

Newcastle Disease (NCD)

West Nile virus can cause a fatal neurological disease in humans. However, approximately 80% of people who are infected will not show any symptoms. In rest 20%, it appears as a mild, non-fatal, febrile, self-limiting illness rarely leading to encephalitis. However some rare non-neurological complication like myocarditis, and pancreatitis have also been reported [25,26]. No vaccine or specific antiviral treatments for West Nile virus infection are available. Over-the-counter pain relievers can be used to reduce fever and relieve some symptoms. In severe cases, patients often need to be hospitalized to receive supportive treatment, such as intravenous fluids, pain medication, and nursing care. For diagnosis, enzyme linked immunosorbant assay, haemagglutination inhibition test, neutralization test and reverse transcriptase – PCR have


After Avian influenza, the other very serious disease that has tremendous impact on poultry health with profound economic consequences in global poultry industry is Newcastle disease. The disease causative agent is a highly variable single stranded RNA virus, avian paramyxovirus serotype 1 virus which, with viruses of the other eight serotypes (avian paramyxovirus 1-9) has been placed in the family Paramyxoviridae. Within the one serotype, pathotypes of Newcastle disease based on clinical signs and lesions vary in virulence and severity from mild subclinical infections (lentogenic) to very virulent (velogenic) strains where mortality approaches 100% [30]. Virulent strains are endemic in poultry in most of Asia, Africa, and some countries of North and South America. It is thought that nearly every species of bird is susceptible and more than 200 susceptible species have been documented [31]. The transmission of virus occurs through respiratory aerosols, exposure to fecal and other excretions from infected birds, through newly introduced birds, selling and giving away sick birds and contacts with contaminated feed, water, equipment and clothing [32]. In poultry, it may take the form of haemorrhagic enteritis and paralysis, or an acute respiratory disease. Although, NCD too has a zoonotic potential, but is much less severe in humans than avian influenza. Newcastle disease virus was first documented as a human zoonosis many decades ago. While mild, self-limiting infections in poultry workers and researchers are occasionally documented, fortunately, the virus does not represent a significant or severe threat to human health and human-to-human spread has never been reported. But, the potential for human to bird transmission exists [33]. Clinical infections in humans usually result from accidental exposure to vaccines or fluids from infected birds or carcasses. Commonly, conjunctivitis develops within 24 hours and is sometimes accompanied by lacrimation, palpebral edema, pain. Rarely, fever, chills, depressed appetite and photophobia has also been reported in humans [34]. Diagnosis relies primarily on history, clinical signs and lesions. All these together may establish a strong index of suspicion but the laboratory con-



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firmation must be done using hemagglutination and hemagglutination inhibition test, virus neutralization test, enzyme linked immune-sorbent assay, plaque neutralization test and reverse-transcriptase PCR. No definite treatment for this disease is known. The general approaches to the prevention and control of Newcastle disease in birds include hygiene and prophylactic measures like vaccination. 1-2 day old chicks should be vaccinated by F-1 vaccine. After about two months, the chicks should be given booster dose using R2B and it is advisable to vaccinate the adult birds at least once a year. The suffering birds should be immediately isolated from the flock. The use of personnel protective equipment and biological safety cabinet has been found suitable in reducing the exposure of laboratory workers to infection. Among poultry farm workers, infection is rarely seen; moreover, persons handling or consuming poultry products do not appear to be at risk [35].

persons annually, or 0.8% of the population [40]. In both developed and developing countries, they cause more cases of confirmed foodborne bacterial diarrhea than Salmonella bacteria [41]. Campylobacteriosis occurs much more frequently (roughly twice) in the summers than in the winters [42]. Infections in humans occur mainly as a result of consumption of uncooked or partially cooked poultry meat which has not been subjected to proper heat treatment and due to handling of contaminated poultry. The non-chlorinated drinking water, unpasteurized milk, contaminated beef and pork products are also responsible for infection in humans. The disease in humans is generally self-limiting (after 3-6 days symptoms usually disappear) but may sometimes leave behind debilitating sequelae with complications like reactive arthritis, Guillain–Barre’ syndrome (GBS), nephritis, myocarditis, pancreatitis or septic abortion. Guillain-Barré Syndrome is a neuropathological disorder characterized by acute ascending

Bacterial Agents Transmissible from Poultry to Humans

bilateral paralysis and it is thought to occur in roughly 1 out of 1,000 reported Campylobacter spp. infections [43]. In a study conducted in New Zealand, it was found that there was Decline in Guillain-Barré Syndrome by 13% after decline in Campylobacteriosis cases by 52% [44]. After the eradication of polio in most parts of the world, GBS has become the most common cause of acute flaccid ascending paralysis [45].

Many bacterial agents affect poultry of all ages and their successful control entails isolating and identifying disease-producing species, if present, and preventing multiplication and spread of the organism within the animal’s body or to other animals. Some common bacterial agents/diseases found in poultry, which can pose significant risks to human health are:

Campylobacteriosis Campylobacteriosis is caused by member of genus Campylobacter (Greek Campylo means curverd; little rods) consisting of 25 species, 8 subspecies and 2 provisional species of which Campylobacter jejuni, C. fetus (subspecies venerealis) and C. coli are of veterinary and human importance [36]. These are thin, sea-gull winged shaped, Gram-negative, motile, non–spore forming, microaerophilic bacterium. Globally, C. jejuni subsp. jejuni is responsible for approx. 95% of all Campylobacter enteritis in humans followed by C. coli (5%). Poultry has been recognized as the primary reservoir of Campylobacter spp. It harbors three different species of this bacterium: Campylobacter jejuni, C. coli, and C. lari but thermophillic C. jejuni and to some extent C. coli are the leading cause of gastroenteritis in humans’ worldwide [37]. It is believed that 80% of broiler flocks are infected with C. jejuni. Once associated with vibrionic hepatits in laying hens, today these bacteria are not important in avian microbiology and pathology; however, they are a source of serious food poisoning in humans [38]. The campylobacters are generally regarded as one of the most common bacterial cause of gastroenteritis worldwide. Its infection has been among the most commonly reported zoonoses in the European countries (1%) followed by Salmonellosis and Yersiniosis [39]. In US from 1997 to 2008, 262 outbreaks with 9135 illnesses, 159 hospitalizations and only 3 deaths were recorded. In India, Campylobacter infections are sporadic in nature but some outbreaks have also been reported at times e.g. in U.P., Haryana etc. [37]. Campylobacteriosis is estimated to affect over 2.4 million


The campylobacter infection is usually self-limiting and supportive therapy includes fluids and electrolytes. Nowadays, erythromycin is the drug of choice and can be used in children, and tetracycline in adults. In some human clinical trials, azithromycin has also been found effective [46]. In severe cases, ciprofloxacin was the drug of choice but there are reports of ciprofloxacin resistant Campylobacter spp., which may have developed due to its unrestricted use and the use of enrofloxacin in poultry [47]. The ubiquity of the bacteria in the environment makes eradication and prevention of infection at the farm level nearly impossible. However, pasteurization of milk, chlorination of drinking water and proper cooking of food especially poultry meat prove beneficial in preventing disease in humans. Infected health care workers should not provide direct patient care and make sure that persons with diarrhea, especially children, wash their hands carefully and frequently with soap to reduce the risk of spreading the infection.

Colibacillosis This is the common name for a large variety of food-or water-borne diseases caused by the bacterium Escherichia coli, which is a part of physiological flora of gastrointestinal tract of all warm blooded animals. Under certain unfavourable conditions such as poor management, poor sanitation, immune deficiency, stress, and viral infection etc., a sudden proliferation of the bacteria takes place which lead to emergence of opportunistic infections [48]. There are a number of different strains, many species-specific. Not all strains are pathogenic. In poultry, E. coli infections are often confounding. These bacteria may be associated with septicemia, chronic



respiratory disease, synovitis (inflammation of the joints which can lead to lameness), pericarditis (inflammation of the sac around the heart), and salphingitis complicated by other syndromes depending on the E. coli serotype. These complications may include fever, dysentery, shock, and purpura (multiple small purplish hemorrhages in the skin and mucous membranes). The incubation period is 12 hours to 5 days, although 1272 hours is most common. Transmission is via the fecal-oral route [49]. In most cases, symptomatic treatment (fluids, antidiarrheals) is all that is required. In more severe infections, antibiotics such as tetracycline and chloramphenicol may be necessary (inflammation of the oviduct). Humans with colibacillosis usually manifest diarrhea which may be, responsible for debilitating symptoms such as gastro-enteritis (diarrhea, vomiting), headaches, and depression, leading sometimes to death. However, most concerning to human health is not the threat of direct infection from poultry sources but the fact that strains of avian pathogenic E. coli share similar serotypes, virulence factors, and genes and plasmids for antibiotic resistance with human strains [50]. There are certain reports, wherein strains with similar virulent and antibiotic resistance factors have been isolated in retail poultry products that cause cystitis and meningitis in people [51]. Recently in Bangladesh, antibiogram profile of E. coli isolates of chicken revealed that it was multidrug resistant (resistant against two antibiotics, such as ampicillin and cefalexin) [52]. Therefore, in today’s scenario where antimicrobial resistance is considered as greatest threat to mankind, isolation of such pathogen sharing common properties is alarming and demands attention.

Salmonellosis Most of the 2,500 strains of Salmonella enterica can infect a wide range of animal species and are capable of causing diarrhoea in humans. Throughout the world, the most important food borne Salmonella strains are Salmonella typhimurium and Salmonella enteritidis, both in terms of number of cases and the severity of infection caused. Birds are well recognized carriers as well as reservoirs of Salmonella serovars. Serovars which are pathogenic for poultry are divided into two categories: the first is serovars specific for poultry (Salmonella pullorum and Salmonella gallinarum), which are usually not pathogenic for humans and other animals but in birds cause high morbidity, carriage, and shedding; and the second category comprises serovars non-specific to birds but pathogenic for humans. The most important serovar in this category is Salmonella enteritidis. Although, Salmonella infections may affect all domestic poultry, but birds usually appear healthy and continue to shed Salmonella serotypes that lead to human illness; additionally, shedding can be intermittent [53]. Salmonella may also contaminate hatching eggs, which results in diarrhoea, depression and death in young chicks. These bacteria are highly infectious and can be transmitted by mice, rats, other birds and/or through contaminated feed. Symptomless adult birds consti-


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tute a human health risk if meat and egg hygiene are not adequate. Prevention of Salmonella infection in poultry birds is often difficult, which could be attributed to its long and often asymptomatic carriage. It is believed that carrier state may last for several days or weeks and even a lifetime for some of the serovars [54]. Food, mainly poultry meat and eggs, plays the most important role in the epidemiology of human salmonellosis. After the incubation period of 8 to 48 h, the infection proceeds mainly in the form of gastroenterocolitis, accompanied by signs such as increased body temperature, chills, and myalgia. Depending on the virulence of the bacteria, they can also produce enterotoxins. Despite awareness of the risk of salmonellosis from handling raw poultry, people are generally not aware that Salmonella can also spread between live poultry and humans. In recent years, in both household and public settings, there are numerous reports of human Salmonella infection which has been linked to contact with live poultry [55,56,57,58]. Human salmonellosis from contact with live poultry is a challenging, yet largely preventable, public health problem. Prevention requires an integrated One Health approach including public and animal health officials collaborating with the other stakeholders.

Avian Tuberculosis Mycobacterium avium infections are found worldwide in a variety of birds ranging from domesticated poultry and game birds to wild and zoological species. Avian tuberculosis is an infectious disease caused by the bacteria Mycobacterium avium subsp. avium serovars 1, 2, and 3. Due to modern managemental practice, it is rarely seen today in commercial flocks but is quite often reported in backyard poultry. In poultry, M. avium forms tubercular nodules in the small intestine which later spread to other organs, particularly spleen liver, and bone marrow. The resulting chronic debilitating disease leads to emaciation and eventual death of affected birds. The agents get transmitted via fecal-oral route to humans. In humans, M. avium infections can cause local wound infections with swelling of regional lymph nodes [31]. The severity of infection is very high in immune-compromised people such as HIV/AIDS patients [59]. Although, most Mycobacterium infections can be treated with antimicrobials but M. avium is highly resistant to some of commonly used antimicrobial agents. Therefore, complete depopulation of affected poultry flocks is generally recommended to prevent its further spread to other birds as well as to susceptible humans.

Protozoan Agents Transmissible from Poultry to Humans Toxoplasmosis Toxoplasmosis, as a zoonotic disease of poultry has not yet established its impact but the recent reports of its seroprevalence in avian species has drawn the attention of many researchers. Toxoplasmosis is a zoonotic disease caused by infection with the protozoan parasite Toxoplasma gondii. It



is an obligate intracellular parasite that infects humans and a broad range of vertebrate hosts. Felids are the definitive host and excrete the infective oocysts in their feces. The transmission of T. gondii occurs by ingestion of oocysts shed from feline feces, by ingestion of T. gondii cysts from chronically infected tissues, or by vertical transmission [60]. T. gondii infections are widely prevalent in human beings and animals worldwide. Foodborne transmission is one of the major sources of T. gondii infection. Humans can become infected by ingesting tissue cysts from undercooked meat, consuming food contaminated with oocysts, or by accidentally ingesting oocysts from the environment [61]. Additionally, ingestion of infected chicken meat can be a source of infection for T. gondii infection in humans and other animals. Between 15 and 85% of the world adult human population is chronically infected with T. gondii depending on the geographical location [62]. One third of the world population has antibody against T. gondii which is an indicator of parasite distribution all around the world. Recent findings indicated that latent toxoplasmosis is not only unsafe for human, but also may play various roles in the etiology of different mental disorders [63]. Estimates suggest that 23% of adolescents and adults are infected with T. gondii, and accounts for 24% of deaths due to foodborne illness in the USA [64]. Toxoplasmosis in human during pregnancy may lead to death of fetus or cause serious defects in fetus [65]. Infection in immunocompromised population may also cause serious problems and sometimes even death [66]. Rarely, toxoplasmosis can cause clinical disease in chickens [67]. Chickens, turkeys, ducks, sparrows and other birds can be infected with T. gondiias intermediate host and acquire infection by digesting infective oocysts shed from the feces of definitive host i.e. felines. Domestic breeding birds and poultries are less infected than free-ranging or industrial breeding since they are not allowed to contact with infective oocysts or feline. Infected birds are considered one of the best indicators for soil contamination with T. gondii oocysts because they feed on the ground [68]. The new trend in the production of free-range organically raised meat could increase the risk of T. gondii contamination of meat, although there is no document about infection transmission by eggs [69,70]. The studies have indicated that prevalence rates in the free-ranging chicken varied from as low as 6.2% in Mexico, 16.9% in Ohio state of the USA, 17.9% in India, 4065.15% in Brazil, 40.4-47.2% in Egypt, and as high as 65.5% in Argentina. In these studies, about 70% isolates from chicken were genotype I and 27% isolates from chicken were genotype III. [60, 65,71,72]. Several serological tests, including the Sabin-Feldman Dye Test (DT), Complement Fixation Test (CFT), complement inhibition test, Indirect Haemagglutination Test (IHAT), Indirect Fluorescent Antibody Test (IFAT), Latex Agglutination Test (LAT), Enzyme-Linked Immunosorbent Assay (ELISA) and the Modified Agglutination Test (MAT) are employed to detect antibodies to T. gondii in sera of chickens [73,74,75]. The presence of cysts in the tissues, bioassays and DNA based tests like polymerase chain reaction are the di-


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agnostic tests employed for the detection of T. gondii in chicken [76,77,78]. T. gondii infection can be prevented by measures to reduce T. gondii in meat; adequate cooking, freezing, or physical/chemical treatment of meat. The organisms in meat can be killed by exposure to extreme cold or heat. Tissue cysts in meat are killed by heating the meat throughout to 67°C and by cooling to −13°C [79]. The cross contamination from raw meat should be prevented. The measures that prevent T. gondii infection of cats, and therefore, decrease spreading of oocysts into the environment (e.g. keeping cats indoors and not feeding raw meat to cats) should be followed. Due to the risk to the fetus, pregnant women should avoid contact with cats, soil, and raw meat. Pet cats should be fed only dry, canned, or cooked food. The cat litter box should be emptied every day [80].

Fungal Agents Transmissible from Poultry to Humans Aspergillosis All domestic poultry, wild birds, other animals and humans can be infected by fungi. The most common fungal disease in birds is aspergillosis. It is an important occupational problem in poultry industry leading to huge economic losses in terms of heavy mortality and morbidity especially in chicks [81]. A wide host range for of this filamentous ubiquitous and opportunistic pathogen has been reported throughout the world. Aspergillus fumigatus is one of the most pathogenic and prevalent species known followed by Aspergillus flavus and Aspergillus niger [82]. Inhalation of spores present in soil, water and feed is one of the most important modes of transmission to affected animals and human beings. This infection usually contracts the people which are immune-compromised or using extensive medications like corticosteroids and antibiotics [83,84]. The zoonotic implication of Aspergillosis is seen more pronounced in workers serving poultry farm, handing the infected birds and their contaminated litter or feed [85]. This fungus and the metabolites produced are quite efficient to produce respiratory form of diseases and can spread to kidneys, liver, intestine, brain and bones through hematogenous route. The diagnosis of this disease is often difficult due to non-specific symptoms depicted by the infected ones and can be best demonstrated by isolation, x-rays and serology [86]. In human beings, granulomatous pulmonary lesions produced by this fungus predispose them to Mycobacterial infections, cerebral lesions, hepatic carcinoma etc. Pulmonary form is most important and common form in human beings as well as animals including poultry and can lead to chronic productive cough, hemoptysis, labored and soundless breathing due to plugs of fungal hyphae or allergic reaction in bronchi [82,87]. The hazardous inter species spread of this fungus can be prevented by proper inspection of litter, feed and water in poultry industry. Use of chlorinated water, cleaned utensils, and timely use of better antifungal agents further can be better alternate to constrict the hazardous outcomes of this fungus. Volume 2; Issue 1; 005


Cryptococcosis An opportunistic and zoonotic yeast Cryptococcus neoformans is documented a long back to be transmitted through inhalation of droppings/ guano of variety of bird species like chickens, pigeons, parrots, canaries etc. [88]. Decaying material of trees (Eucalyptus) along with droppings is also supposed to be the major carrier of C. gatti. A variety of animal species including dogs, horses, donkeys, felids, cattle, sheep, goats, pigs and wild animals are found to be affected by this fungus. But in birds the clinical outcome of the infection is rarely seen [89]. In spite of species variation Cryptococcus neoformans and Cryptococcus gattii are major fungal forms associated with casualties. The immune-compromised people with defective cell mediated immunity are the major victims affected with this infection i.e. AIDS patients, recipients of organ transplants etc. Although the infection has been reported to affect immune-competent individuals as well as reported by [90], where a patient exposed to a pet bird pica (magpie) acquired the infection. This organism undergoes colonization in the nasal cavity of affected beings and can lead to the formation of fungal granulomas in different organs. Occasionally the transmission through abraded skin, nosocomial route, direct contact, organ transplant, mammary gland has also been reported in animals. The infection usually led to the development of nervous signs in individuals as the agent causes encephalomyelitis in human beings [90]. The symptomatic diagnosis of infection is difficult, as non-specific clinical manifestations like dyspnoea, anorexia, diarrhoea, paralysis, blindness are evident in the patient. But necropsy examination often reveals presence of myxomatous deposits in brain, respiratory tract and abdominal cavity [90-92]. Prognosis of this infection is poor in affected individuals, so precautionary measures are suitable assets. Prevention can be implemented by adequate ventilation in farms, proper disposal or incarnation of droppings of birds, tree trunks, nests and perches [93].

Histoplasmosis Histoplasmosis is an infectious, granulomatous and non-contagious disease of man, dog, horse, cattle, sheep and wild animals. Although dogs are most susceptible to this infection, Histoplasma capsulatum is an important pathogenic opportunistic fungal species which is transmitted to human beings through soil contaminated with the droppings of birds around their nests or caves. Inhalation of spores from infected soil serves as a most potent mode of transmission to human beings and other animals [94]. Although this infection is not of much economic significance to poultry industry but its zoonotic implication throws lime light on its transmission by poultry. This fungus usually proliferate within macrophages and leads to extensive proliferation of reticuloendothelial cells [95]. Classical granuloma in lungs composed of giant cells is characteristic feature of this infection. In histoplasmosis acute to chronic pneumonia, cutaneous ulcers and lymphadenopathy in human beings are often evi-


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dent. Lymphadenopathy is again a feature associated with extensive reticuloendothelial cell proliferation. Like Cryptococcus the incidence of this infection is also more reported in old age groups or persons affected with immunosuppressive diseases like AIDS [96]. Acute and chronic pulmonary histoplasmosis, progressive disseminated histoplasmosis and mediastinal lymphadenitis are various forms of this infection [97]. The diagnosis of this organism is based upon Periodic Acid-Schiff (PAS), Gomori Methenamine-Silver Nitrate Stain (GMS) and Bauer staining methods. Other associated techniques involve complement fixation test, agar plate precipitation test, cultural isolation and skin test with histoplasmin [98]. Preventive measures include avoiding exposure to dropping of infected birds, use of protective coats while dealing with birds in poultry industries or farms. Amphotericin B is considered as a best treatment of choice for the patients infected with this deadly fungal infection and Fluconazole is less effective than Amphotericin B [99,100].

Chlamydial Agents Transmissible from Poultry to Humans Chlamydiosis Chlamydiosis (ornitosis or psittacosis or parrot fever) is a complex, occupational, emerging zoonotic infection caused by Chlamydia psittaci (non-motile, intracellular bacteria) which can affect birds (psittacine as well as non-psittacine through natural infection), mammalian species as well as human beings [101]. Pet birds are supposed to be an important reservoirs for Chlamydia induced infections to human beings and reported from India first time by [101] and globally first report was recorded in year 1893 [102]. The infection is usually sub-clinical in birds (wild as well as domestic) but spread the infection amongst workers in poultry processing plants, veterinarians and bird dealers [103,104]. Inhalation of organism shed by infected birds, handing of dead infected birds, nasal discharge, bite, person to person contact are the pivot modes of transmission of this infection to human beings. The zoonotic implication of this disease can often be assessed by many global outbreaks indicating flu like clinical manifestations in human beings and the magnitude of pathogenic potential has been found to be more pronounced in pregnant ladies [105,106]. In human Chlamydiosis leads to fever, respiratory symptoms (pharyngitis, dyspnoea, pneumonia, bradycardia), photophobia, diarrhoea, splenomegaly and other complications like conjunctivitis, arthritis, endocarditis, encephalitis and fetal death [107,108]. In animals, respiratory distress, conjunctivitis, fibrinous pericarditis, pleurisy, enteritis, polyarthritis are important recorded manifestations [101]. Diagnosis of this infection is based upon the cultural isolation, serology and molecular tools and isolation needs biosafety level 3. Detection of intra-cytoplasmic inclusions in tissues or exudates by Gimenz or Giemsa stains, serological tests like ELISA, CFT, Microimmunofluorescence (MIF) and DNA probe can be helpful [107]. But the samples for error free diagnosis must be collected before the start of antibiotic treatment. TetraVolume 2; Issue 1; 005


cyclines are the drug of choice for the treatment of affected individuals but patient must take the treatment up to 21 days to reduce the risk of further relapse or spread [107]. Non-availability of any potent vaccine and lack of awareness makes it difficult to eliminate this infection successfully. So the deadly outcomes of this infection can be prevented by notifying such disease like other countries (Hong Kong) [107]. Protective clothing to workers in poultry farm, poultry processing plants and pet bird handlers; proper disposal and collection of autopsy samples from dead and infected birds; distinction of area where the aborted animals or affected birds are kept; adoption and surveillance regarding hygiene to prevent the spread of infection are important preventive tools which can prevent the spread of infection.

References: 1.

World Health Organization (2006) The Control of Neglected Zoonotic Diseases: A route to poverty alleviation Geneva. Report of a joint WHO/DFID-AHP meetings with the participation of FAO and OIE, Geneva, 20-21 September 2005.

2.

Molyneux D, Hallaj Z, Keusch GT, McManus DP, Ngowi H, et al. (2011) Zoonoses and marginalized infectious diseases of poverty: Where do we stand? Parasites and Vectors 4: 106.

3.

Anonymous (2017) Press Information Bureau, Government of India, Ministry of Agriculture & Farmers Welfare.

4.

Samorek-Salamonowicz E, Wijaszka T, Kozdruń W (2006) Zoonotic aspects of avian influenza. Post Mikrobiol 45(Suppl): 39–49.

5.

Fouchier RA, Munster VJ (2009) Epidemiology of low pathogenic avian influenza viruses in wild birds. Rev Sci Tech 28(1): 49-58.

6.

Reed KD, Meece JK, Henkel JS, Shukla KS (2003) Birds, migration and emerging zoonoses: West Nile virus, Lyme disease, influenza A and enteropathogens. Clin Med Res 1(1):5-12.

7.

Wanaratana S, Panyim S, Pakpinyo S (2011) The potential of house flies to act as a vector of avian influenza subtype H5N1 under experimental conditions. Med Vet Entomol 25(1): 58-63.

8.

Capua I, Marangon S (2000) The avian influenza epidemic in Italy, 1999–2000: a review. Avian Pathol 29(4): 289-294.

9.

Swayne DE, Suarez DL (2000) Highly pathogenic avian influenza. Rev Sci Technol 19(2): 463-468.

Conclusion With the escalating demand of organic and nutritious food, developments in food science and technology, liberalization of food trade and growing awareness towards public health, it becomes essential to produce and supply quality products. Therefore, to ensure the healthy status of poultry industry, it is important that birds should be kept in good health and all the measures to prevent the introduction and spread of harmful biological substances in the poultry population should be carefully designed. Hence, biosecurity measures acts as a cornerstone for reaping the maximal benefits out of this profitable enterprise. Various infectious agents are continuously diagnosed in poultry species. Although, frequency of disease transmission from birds to humans is low, but the diseases crossing the species barrier always pose a significant public health risk to especially occupationally exposed people like veterinarians and health care providers and YOPI (Young, Old and Ill people) along with their economic consequences. Control/prevention of zoonotic diseases and protection of public health are challenging tasks as the world population is increasing proportionately. The prevention of these infections depends on improved diagnosis and highly effective therapeutics/prophylactics. The collective effort of professionals from medical and veterinary and others is necessary to combat these zoonotic infections. Therefore, an integrated One Health approach involving the poultry industry, feed manufacturers, healthcare providers, backyard flock rears and veterinarians, and is needed to help prevent spread of avian zoonotic diseases.

Conflict of Interest The authors declare no conflict of interest.

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10. World Organization for Animal Health (OIE) (2014) Terrestrial animal health code [online]. Paris: OIE; 2014. Avian influenza. 11. Yu H, Cowling BJ, Feng L, Lau EH, Liao Q, et al. (2013) Human infection with avian influenza A H7N9 virus: an assessment of clinical severity. Lancet 382(9887): 138-145. 12. Uyeki TM (2009) Human infection with highly pathogenic avian influenza A (H5N1) virus: review of clinical issues. Clin Infect Dis 49(2): 279-290. 13. Shi J, Xie J, He Z, Hu Y, He Y, et al. (2013) A detailed epidemiological and clinical description of 6 human cases of avian-origin influenza A (H7N9) virus infection in Shanghai. PLoS One 8(10): e77651. 14. Centers for Disease Control and Prevention [CDC] (2014) Avian flu [Website online]. CDC; 2014 Jan. 15. Cardona C, Slemons R, Perez D (2009) The prevention and control of avian influenza: The avian influenza coordinated agriculture project, Poultry Science 88(4): 837-841.




16. Smithburn KC, Hughes TP, Burke AW, Paul JH (1940) A neurotropic virus isolated from the blood of a native of uganda. Am J Trop Med 20: 471-492. 17. Tsai TF, Popovici F, Cernescu C, Campbell GL, Nedelcu NI (1998) West Nile encephalitis epidemic in southeastern Romania. Lancet 352(9130): 767–771. doi: 10.1016/S0140-6736(98)03538-7 18. Weinberger M, Pitlik SD, Gandacu D, Lang R, Nassar F, et al. (2001) West Nile fever outbreak, Israel, 2000: epidemiologic aspects. Emerg Infect Diseases 7(4): 686-691. 19. Komar N (2000) West Nile viral encephalitis. Rev Sci Tech 19(1): 166-176. 20. Murgue B, Murri S, Zientara S, Durand B, Durand J, et al. (2001) West Nile outbreak in horses in southern France, 2000: The return after 35 years. Emerg Infect Dis 7(4): 692-696. 21. George S, Gourie-Devi M, Rao JA, Prasad SR, Pavri KM (1984) Isolation of West Nile virus from the brains of children who had died of encephalitis. Bull World Health Organ 62(6): 879-882. 22. Rodrigues FM, Guttikar SN, Pinto BD (1981) Prevalence of antibodies to Japanese encephalitis and West Nile viruses among wild birds in the Krishna-Godavari Delta, Andhra Pradesh, India. Trans R Soc Trop Med Hyg 75(2): 258–262. doi: 10.1016/00359203(81)90330-8

Page 12 of 13

control. J Vet Diag Invest 23(4): 637-656. 31. Dale E, Brown C (2013) Zoonotic Diseases from Poultry. Braz J Vet Pathol 6(2): 76-82. 32. Abdisa T, Tagesu T (2017) Review on Newcastle Disease of Poultry and its Public Health Importance. J Vet Sci Technol 8: 441. doi:10.4262/2157-7579.1000441 33. Alexander DJ (2000) Newcastle disease and other avian paramyxoviruses. Rev Sci Tech 19(2): 443-462. 34. Swayne DE, King DJ (2003) Zoonosis Update: avian influenza and Newcastle disease. J. Am Vet Med Assoc 222: 1534-1540. 35. Nolen RS (2003) Emergency declared: exotic Newcastle disease found in commercial poultry farms. J Am Vet Med Assoc 222(4): 411. 36. Man SM (2011) The clinical importance of emerging Campylobacter species. Nat Rev Gastroenterol. Hepatol 8(12): 669-685. 37. Malik H, Kumar A, Rajagunalan S, Kataria JL, Anjayet al. (2014) Prevalence of Campylobacter jejuni and Campylobacter coli among broilers in Bareilly region. Veterinary World 7(10): 784-787. 38. Peckham MC (1958) Avian vibrionic hepatitis. Avian Dis 2(3): 348358.

23. Weese JS, Baird JD, DeLay J, Kenney DG, Staempfli HR, et al. (2003) West Nile virus encephalomyelitis in horses in Ontario: 28 cases. The Canadian Veterinary Journal 44(6): 469-473.

39. European Food Safety Authority (EFSA) (2010) The community summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in the European Union in 2008. EFSA J 8: 1496-1906.

24. Benjelloun A, Harrak ME, Calistri P, Loutfi C, Kabbaj H, et al. (2017) Seroprevalence of West Nile virus in horses in different Moroccan regions. Veterinary Medicine and Science 3(4): 198-207.

40. Salim SM, Mandal J, Parija SC (2014) Isolation of Campylobacter from Human Stool Samples. Indian Journal of Medical Microbiology 32(1): 35-38.

25. Albagal C, Chaimoff R (1959) A case of West Nile myocarditis. Harcfach 57: 274.

41. Bolton DJ (2015) Campylobacter virulence and survival factors. Food Microbiology 48: 99-108.

26. Perelman A, Stern J (1974) Acute Pancreatitis in West Nile fever. Am J Trop Med Hyg 23(6): 1150-1152.

42. Vaishnavi C, Singh M, Thakur JS, Thapa BR (2015) Low Prevalence of Campylobacteriosis in the Northern Region of India. Advances in Microbiology 5(3): 155-165.

27. Khan SA, Chowdhury P, Choudhury P, Dutta P (2017) Detection of West Nile virus in six mosquito species in synchrony with seroconversion among sentinel chickens in India. Parasites & Vectors 10: 13. doi:10.1186/s13071-016-1948-9 28. Laird M, Miles JW (1985) Integrated mosquito control methodologies, 2 vols, London, Academic Press, Inc.; 1983-1985. 29. Paramasivan R, Mishra AC, Mourya DT (2003) West Nile virus: the Indian scenario. Indian J Med Res 118: 101-108. 30. Cattoli G, Susta L, Teregino C, Brown C (2011) Newcastle disease: A review of field recognition and current methods of laboratory BAOJ Vet Sci, an open access journal

43. Yuki N, Susuki K, Koga M, Nishimoto Y, Odaka M, et al. (2004) Carbohydrate mimicry between human ganglioside GM1 and Campylobacter jejuni lipooligosaccharide causes Guillain–Barré syndrome. Proc Natl Acad Sci 101(31): 11404-11409. 44. Baker MG, Kvalsvig A, Zhang J, Lake R, et al. (2012) Declining Guillain-Barré Syndrome after Campylobacteriosis Control, New Zealand, 1988–2010. Emerging Infectious Diseases 18(2): 226-233. 45. Nachamkin I, Allos BM, Ho T (1998) Campylobacter Species and Guillain-Barre´ Syndrome. Clinical Microbiology Reviews 11(3): 555-567. Volume 2; Issue 1; 005


46. Vukelic D, Trkulja V, Salkovic-Petrisic M (2010) Single oral dose of azithromycin versus 5 days of oral erythromycin or no antibiotic in treatment of campylobacter enterocolitis in children: a prospective randomized assessor-blind study. J Pediatr Gastroenterol Nutr 50(4): 404-410. doi: 10.1097/MPG.0b013e3181a87104 47. Agunos A, Léger D, Avery BP, Parmley EJ, Deckert A, et al. (2013) Ciprofloxacin-Resistant Campylobacter spp. in Retail Chicken, Western Canada. Emerging Infectious Diseases 19(7): 1121-1124. doi:10.3201/eid1907.111417 48. Kozdrun W, Czekaj H, Stys N (2015) Avian zoonoses - a review. Bull Vet Inst Pulawy 59: 171-178 49. Smigielska M (2010) Zoonoses of free-living birds. Ornis Polonica 51: 149-162. 50. Lima-Filho JV, Martins LV, Nascimento DC, Ventura RF, Batista JE, et al. (2013) Zoonotic potential of multidrug-resistant extraintestinal pathogenic Escherichia coli obtained from healthy poultry carcasses in Salvador, Brazil. Braz J Infect Dis 17(1): 54-61. 51. Johnson JR, Delavari P, O’bryan TT, Smith KE, Tatini S (2005) Contamination of retail foods, particularly turkey, from community markets (Minnesota, 1999-2000) with antimicrobial-resistant and extraintestinal pathogenic Escherichia coli. Foodborne Pathog Dis 2(1): 38-49. 52. Matin MA, Islam MA, Khatun MM (2017) Prevalence of colibacillosis in chickens in greater Mymensingh district of Bangladesh. Veterinary World 10(1): 29-33. doi: 10.14202/ vetworld.2017.29-33 53. Centers for Disease Control and Prevention (CDC) (2009) Centers for Disease Control and Prevention. Multistate outbreaks of Salmonella infections associated with live poultry—United States, 2007. MMWR Morb Mortal Wkly Rep 58(2): 25-29.

Page 13 of 13

contact with baby poultry from a single agricultural feed store chain and mail-order hatchery, 2009. Pediatr Infect Dis J 32(1): 8-12. 58. Hedican E, Miller B, Ziemer B, LeMaster P, Jawahir S , et al. (2010) Salmonellosis outbreak due to chicken contact leading to a foodborne outbreak associated with infected delicatessen workers. Foodborne Pathog Dis 7(8): 995-997. 59. Von Reyn CF, Arbeit RD, Horsburgh CR, Ristola MA, Waddell RD, et al. (2002) Sources of disseminated Mycobacterium avium infection in AIDS. J Infect 44(3): 166-170. 60. Jones JL, Dubey JP (2012) Foodborne Toxoplasmosis. Clinical Infectious Diseases 55(6): 845-851. 61. Tenter AM, Heckeroth AR, Weiss LM (2000) Toxoplasma gondii: from animals to humans. Int J Parasitol 30(12-13): 1217-1258. 62. Fuentes I, Rubio JM, Ramírez C, Alvar J (2001) Genotypic Characterization of Toxoplasma gondii Strains Associated with Human Toxoplasmosis in Spain: Direct Analysis from Clinical Samples. Journal of Clinical Microbiology 39(4): 1566-1570. 63. Dalimi A, Abdoli A (2012) Latent Toxoplasmosis and Human. Iran J Parasitol 7(1): 1-17. 64. Hughes JM, Colley DG, Lopez A, Dietz VJ (2000) Preventing congenital toxoplasmosis. Morb Mortal Weekly Report 49(2): 5775. 65. Singh S (2016) Congenital toxoplasmosis: Clinical features, outcomes, treatment, and prevention. Trop Parasitol 6(2): 113-122. 66. Basavaraju A (2016) Toxoplasmosis in HIV infection: An overview. Trop Parasitol 6(2): 129-135. 67. Dubey JP (2009) Toxoplasma gondii Infections in Chickens (Gallus domesticus): Prevalence, Clinical Disease, Diagnosis and Public Health Significance. Zoonoses and Public Health 57(1): 60-73.

54. Behravesh CB, Brinson D, Hopkins BA, Gomez TM (2014) Backyard Poultry Flocks and Salmonellosis: A Recurring, Yet Preventable Public Health Challenge. Clinical Infectious Diseases 58(10):1432-1438.

68. Azar S, Mehdi S, Hosseini TS, Shahabeddin S, Rahimi MT, et al. (2017) Birds and poultries toxoplasmosis in Iran: A systematic review and meta-analysis. Asian Pacific Journal of Tropical Medicine 10(7): 635-642.

55. Gaffga N, Barton Behravesh C, Ettestad P, Smelser CB, Rhorer AR, et al. (2012) Outbreak of salmonellosis linked to live poultry from a mail-order hatchery. N Engl J Med 366: 2065-2073.

69. Hussain MA, Stitt V, Szabo Elizabeth A, Nelan B (2017) Toxoplasma gondii in the Food Supply. Pathogens 6(2): 21. 70. Jones JL, Holland GN (2010) Annual burden of ocular toxoplasmosis in the United States. Am J Trop Med Hyg 82(3): 464-465.

56. Loharikar A, Briere E, Schwensohn C, Weninger S, Wagendorf J, et al. (2012) Four multistate outbreaks of human Salmonella infections associated with live poultry contact, United States, 2009. Zoonoses and Public Health 59(5): 347-354.

71. Dubey JP, Beattie CP (2010) Toxoplasmosis of Animals and Man (2nd edn.) CRC Press, Florida, Boca Raton. pp. 336.

57. Loharikar A, Vawter S, Warren K, Deasy M, Moll M, et al. (2013) Outbreak of human Salmonella Typhimurium infections linked to

72. Dubey JP (2010) Toxoplasmosis of animals and humans (2nd edn.). CRC Press, Boca Raton, Florida: 1-313.




Page 14 of 13

73. Ferraroni JJ, Reed SG, Speer CA (1980) Prevalence of Toxoplasma antibodies in humans and various animals in the Amazon. The Helminthological Society of Washington 47(1): 148-150.

87. Bennett JE (1980) Aspergillosis, 742-744. In KJ Isselbacher KJ, Adams RD, Braunwald E, Petersdorff RG, and Wilson JD (eds.), Harrison’s Principles of Internal Medicine, McGraw-Hill, New York.

74. Zia-Ali N, Fazaeli A, Khoramizadeh M, Ajzenberg D, Dardé M, et al. (2007) Isolation and molecular characterization of Toxoplasma gondii strains from different hosts in Iran. Parasitol Res 101(1): 111115.

88. Micalizzi C, Persi A, Parodi A (1997) Primary cutaneous cryptococcosis in an immunocompetent pigeon keeper. Clin Exp Dermatol 22(4): 195-197.

75. Dubey JP, Venturini MC, Venturini L, Piscopo M, Graham DH, et al. (2003) Isolation and genotyping of Toxoplasma gondii from freeranging chickens from Argentina. J Parasitol 89(5): 1063-1064.

89. Irokanulo EOA, Makinde AA, Akuesgi CO, Ekwonu M (1997) Cryptococcus neoformans var neoformans isolated from droppings of captive birds in Nigeria. J Wildl Dis 33(2): 343-345.

76. Sreekumar C, Graham DH, Dahl E, Lehmann T, Raman M, et al. (2003) Genotyping of Toxoplasma gondii isolates from chickens from India. Vet Parasitol 118(3-4): 187-194.

90. Lagrou K, Eldere JV, Keuleers S, Hagen F, Merckx R, et al. (2005) Zoonotic transmission of Cryptococcus neoformans from a magpie to an immunocompetent patient. Journal of Internal Medicine 257: 385-388.

77. Burg JL, Grover CM, Pouletty P, Boothroyd JC (1989) Direct and sensitive detection of a pathogenic protozoan, Toxoplasma gondii, by polymerase chain-reaction. J Clin Microbiol 27(8): 1787-1792.

91. Ritchie BW, Dreesen DW (1988) Avian Zoonoses: proven and potential diseases. Part II. Viral, fungal, and miscellaneous diseases. Compend Small Anim 10: 690-695.

78. Mose JM, Kagira J M, Karanja SM, Ngotho M, et al. (2016) Detection of Natural Toxoplasma gondii Infection in Chicken in Thika Region of Kenya Using Nested Polymerase Chain Reaction. Biomed Res Int 7589278.

92. McCluggage DM (1996) Zoonotic Disorders. In: Rosskopf WJ Jr, Woerpel RW (eds). Diseases of Cage and Aviary Birds, (3rd edn). Williams & Wilkins, New York: 535-547.

79. Kotula AW, Dubey JP, Sharar AK, Andrew CD, Shen SK, et al. (1991) Effect of freezing on infectivity of Toxoplasma gondii tissue cysts in pork. Journal of Food Protection 54(9): 687-690. 80. Foulon W, Naessens A, Ho-Yen D (2000) Prevention of congenital toxoplasmosis. J Perinat Med 28(5): 337-345. 81. Leishangthem GD, Singh ND, Brar RS, Banga HS (2015) Aspergillosis in Avian Species: A Review. Journal of Poultry Science and Technology 3(1): 1-14. 82. Cacciuttolo E, Rossi G, Nardoni S, Legrottaglie R, Mani P (2009) Anatomopathological aspects of avian aspergillosis. Veterinary Research Communication 33(6): 521-527. 83. Kliasova GA, Petrova NA, Galstian GM, Gotman LN, Vishnevskaia ES, et al. (2003) Invasive aspergillosis in immunocompromised patients. Ter Arkh 75(7): 63-68. 84. Cray C (2011) Infectious and zoonotic disease testing in pet birds. Clin Lab Med 31(1):71-85. 85. Lobna, Salem MA, Ali AF (2014) Epidemiological study of Aspergillosis in chickens and human contacts in chicken farms at Kalyoubia Governorate. IOSR Journal of Agriculture and Veterinary Science 7(7): 20-24. 86. Acha PN, Szyfres B (2006) Aspergillosis (3rd Edn.) (1): 305-310.


93. Raso TF, Werther K, Miranda ET, Mendes-Giannini MJS (2004) Cryptococcosis outbreak in psittacine birds in Brazil. Medical Mycology 42(4): 355-362. 94. Falci DR, Hoffmann ER, Paskulin DD, Pasqualotto AC (2017) Progressive disseminated histoplasmosis: a systematic review on the performance of non-culture-based diagnostic tests. Braz J Infect Dis 21(1): 7-11. 95. Newman SL (2001) Cell-mediated immunity to Histoplasma capsulatum. Semin Respir Infect 16(2): 102-108. 96. Wheat LJ, Connolly-Stringfield PA, Baker RL, Curfman MF, Eads ME, et al. (1990) Disseminated histoplasmosis in the acquired immune deficiency syndrome: clinical findings, diagnosis and treatment, and review of the literature. Medicine (Baltimore) 69(6): 361-374. 97. Schwarz J, Silverman FN, Adriano SM, Straub M, Levine S (1955) The relation of splenic calcification to histoplasmosis. The New England Journal of Medicine 252(21): 887-891. 98. Gomez BL, Figueroa JI, Hamilton AJ, Ortiz BL, Robledo MA, et al. (1997) Development of a novel antigen detection test for histoplasmosis. J Clin Microbiol 35(10): 2618-2622. 99. Troillet N, Llor J, Kuchler H, Deleze G, Praz G (1996) Disseminated histoplasmosis in an adopted infant from El Salvador. Eur J Pediatr 155(6): 474-476.



Page 15 of 13

100. Bradsher RW (1996) Histoplasmosis and blastomycosis. Clin Infect Dis 22(suppl 2): S102-111.

Alappuzha district, Kerala. The Indian Journal of Medical Research 146(Supplement): S70-S75.

101. Pal M (2017) Chlamydophila Psittaci as an Emerging Zoonotic Pathogen of Global Significance. Int J Vaccines Vaccin 4(3): 80.

117. Khan SA, Chowdhury P, Choudhury P, Dutta P (2017) Detection of West Nile virus in six mosquito species in synchrony with seroconversion among sentinel chickens in India. Parasites and Vectors 10:13.

102. Pal M, Dahiya SM (1985) Occurrence of chlamydial infection in parrots. Indian Journal of Animal Research 19: 69-72.7. 103. Trávnicek M, Cisláková L, Deptuła W, Stosik M, Bhide MR (2002) Wild pigeons and pheasants - a source of Chlamydophila psittaci for humans and animals. Ann Agric Environ Med 9(2): 253-255. 104. Pal M (2013) Public health concern due to emerging and reemerging zoonoses. Int J Livest Res 3(1): 56-62. 105. Lagae S, Kalmar I, Laroucau K, Vorimore F, Vanrompay D (2014) Emerging Chlamydia psittaci infections in chickens and examination of transmission to humans. J Med Microbiol 63(Pt3): 399-407. 106. Tontis A, Zwahlen R (1991) Chlamydia infections in sheep and goats with a reference to its significance as a zoonosis. Tierarztl Prax 19(6): 617-623. 107. Chau S, Tso EY, Leung WS, Fung KS (2015) Three cases of atypical pneumonia caused by Chlamydophila psittaci. Hong Kong Med J 21(3): 272-275. 108. Pal M (2004) Chlamydiosis: An anthropozoonosis. Veterinary World 3: 5-7. 109. APEDA 2016. 110. Nagarajan S, Kumar M, Murugkar HV, Tripathi S, Shukla S, et al. (2017) Novel reassortant highly pathogenic avian influenza (H5N8) virus in zoos, India. Emerging Infectious Diseases 23(4): 717-719. 111. WHO 2017. 112. OIE, WAHIS interface. 113. WHO 2017. 114. Mishra N, Kalaiyarasu S, Nagarajan S, Rao MV, George A, et al. (2012) Serological evidence of West Nile virus infection in wild migratory and resident water birds in Eastern and Northern India. Comparative Immunology and Microbiology of Infectious Diseases 35(6): 591-598. 115. Kalaiyarasu S, Mishra N, Khetan RK, Singh VP (2016) Serological evidence of widespread West Nile virus and Japanese encephalitis virus infection in native domestic ducks (Anas platyrhynchos var domesticus) in Kuttanad region, Kerala, India. Comparative Immunology and Microbiology of Infectious Disease 48: 61-8. 116. Balakrishnan A, Thekkekare RJ, Sapkal G, Tandale BV (2017) Seroprevalence of Japanese encephalitis virus & West Nile virus in BAOJ Vet Sci, an open access journal

118. Alexander DJ (2000) Newcastle disease and paramyxoviruses. Rev Sci Tech 19(2): 443-462.

other

avian

119. Nolen RS (2003) Emergency declared: exotic Newcastle disease found in commercial poultry farms. Journal of American Veterinary Medical Association 222(4): 411. 120. Goebel SJ, Taylor J, Barr BC, Kiehn TE, Castro-Malaspina HR, et al. (2007) Isolation of avian paramyxovirus 1 from a patient with a lethal case of pneumonia Journal of Virology 81(22): 12709-12714. 121. Kaakoush NO, Castaño-Rodríguez N, Mitchell HM, Man SM (2015) Global Epidemiology of Campylobacter Infection. Clinical Microbiology Reviews 28(3): 687-720. doi:10.1128/CMR.00006-15 122. Rajendran P, Babji S, George A, Rajan D, Kang G, et al. (2012) Detection and species identification of Campylobacter in stool samples of children and animals from Vellore, South India. Indian J Med Microbiol 30(1): 85-88. doi:10.4103/0255-0857.93049 123. Wei W, Schüpbach G, Held L (2015) Time-series analysis of Campylobacter incidence in Switzerland. Epidemiology and Infection 143(9): 1982-1989. doi:10.1017/S0950268814002738 124. Scott MK, Geissler A, Poissant T, DeBess E, Melius B, et al. (2015) Campylobacteriosis outbreak associated with consuming undercooked chicken liver pâté — Ohio and Oregon, December 2013–January 2014. Morb Mortal Wkly Rep 64(14): 399. 125. Coura FM, Diniz SA, Silva XM, et al. (2017) Phylogenetic group of Escherichia coli isolates from broilers in Brazilian poultry slaughterhouse. Scientific World Journal 2017: 1-7. doi:10.1155/2017/5898701 126. Stromberg ZR, Johnson JR, Fairbrother JM, Kilbourne J, Van Goor A, et al. (2017) Evaluation of Escherichia coli isolates from healthy chickens to determine their potential risk to poultry and human health. PLoS One 12(7): e0180599 127. Boro SK, Pathak DC, Saikia GK, Buragohain M (2018) Prevalence of olibacillosis in birds in and around Guwahati city (Assam). Journal of Entomology and Zoology Studies 6(1): 1000-1003. 128. Kalaba V, Golić B, Sladojević Z, Kalaba D (2017) Incidence of Salmonella Infantis in poultry meat and products and the resistance of isolates to antimicrobials. IOP Conf Ser Earth Environmental Science 85: 012082. Volume 2; Issue 1; 005


Page 16 of 13

129. Arora D, Kumar S, Jindal N, Narang G, Kapoor PK, et al. (2015) Prevalence and epidemiology of Salmonella enterica serovar Gallinarum from poultry in some parts of Haryana, India. Veterinary World 8(11): 1300-1304.

137. Vieira FEG, Sasse JP, Minutti AF, Miura AC, de Barros LD, et al. (2018) Toxoplasma gondii: prevalence and characterization of new genotypes in free-range chickens from south Brazil. Parasitol Res 117(3): 681-688.

130. Waghamare RN, Paturkar AM, Zende RJ, Vaidya VM, Gandage RS, et al. (2017) Studies on occurrence of invasive Salmonella spp. from unorganized poultry farm to retail chicken meat shops in Mumbai city, India. Int J Curr Microbiol App Sci 6(5): 630-41.

138. Lobna MA, Salem, Ali AF (2014) Epidemiological study of Aspergillosis in chickens and human contacts in chicken farms at Kalyoubia Governorate IOSR Journal of Agriculture and Veterinary Science 7 (7): 20-4.

131. Asakura T, Ishii M, Haraguchi M, Kamiyama I, Kohno M, et al. (2015) Dry pleurisy complicating solitary pulmonary nodules caused by Mycobacterium avium: a case report. J Med Case Rep 9: 238. doi: 10.1186/s13256-015-0723-4

139. Kuroki, Phichaichumpon C, Yasuoka A, Chiranairadul P, Chosa T, et al. (2004) Environmental isolation of Crypptoccocus neoformans from an endemic region of HIV associated cryptococcosis in Thailand. Yeast 21(10): 809-812.

132. Yoon HJ, Chung MJ, Lee KS, Kim JS, Park HY, et al. (2016) Broncho-pleural fistula with hydropneumothorax at CT: Diagnostic implications in Mycobacterium avium complex lung disease with pleural involvement. Korean Journal of Radiology 17(2): 295-301. doi:10.3348/kjr.2016.17.2.295

140. Pervez MM, Cobb B, Matin N, Shahrin L, Ford ER, et al. (2010) Disseminated Histoplasmosis in patient with advanced HIV disease-Lessons learnt from Bangladesh. Journal of Heath Popul Nutr 28(3): 305-307.

133. Deyab AK, Hassanein R (2005) Zoonotic toxoplasmosis in chicken. Journal of Egyptian Society of Parasitology 35(1): 341-350.

141. Oladele RO, Olusola OA, Malcolm DR, David WD (2018) Histplasmosis in Africa: An emerging or neglected disease? PLoS Neglected Tropical Disease 12(1): e0006046.

134. Liu XC, He Y, Han DG, Zhang ZC, Li K, et al. (2017) Detection of Toxoplasma gondii in chicken and soil of chicken farms in Nanjing region, China. Infectious Diseases of Poverty 6(1): 62.

142. Chau S, Tso EY, Leung WS, Fung KS (2015) Three cases of atypical pneumonia caused by Chlamydophila psittaci. Hong Kong Med J 21(3): 272-275.

135. Mose JM, Kagira JM, Karanja SM, Ngotho M, Kamau DM, et al. (2016) Detection of natural Toxoplasma gondii infection in chicken in Thika region of Kenya using nested polymerase chain reaction. BioMed Research International Article ID 7589278.

143. Chan J, Bridget D, James B, Vicky S, Melinda G, et al. (2017) An outbreak of psittacosis at veterinary school demonstrating a novel source of infection. One Health 3: 29-33.

136. Vismarra A, Mangia C, Barilli E, Brindani F, Bacci C, et al. (2016) Meat juice serology for Toxoplasma gondii infection in chickens Ital J Food Saf 5(1): 5586.

