Introduction
Zoonotic diseases are infectious diseases which can be transmitted from animals to man. Due to frequent contact and domestication of wildlife animals, zoonotic diseases are increasingly becoming more prevalent. Public parks and gardens are home to abundant populations of birds. One of the most frequent species known to thrive in such areas are feral pigeon (Columba livia). Although there are few reports of disease transmission between pigeons and humans, their close interaction with humans and ability to carry zoonotic pathogens make them a public health risk. In fact, these birds are present at very high densities (2,000 individuals per km2) and can cover a maximum distance of 5.29 km (Dickx et al., 2010). This may result in the increase risk of pathogen transmission among other birds and potentially to humans. Studies have shown that most infected pigeons do not show signs of clinical disease. These birds may therefore pose a public health risk to the human population.
Pigeons, like many other bird species, can harbor diseases that can be zoonotic in nature. One of the pathogens most frequently carried by pigeons is Chlamydophila psittaci. C. psittaci is an obligate intracellular bacterium that causes a disease in birds known as Psittacosis or Avian Chlamydiosis. Psittacosis is highly contagious and often causes influenza-like symptoms, severe pneumonia and non-respiratory health problems. Birds can shed this bacterium in the environment when they are either overtly ill or without any symptoms. C. psittaci occurs most frequently in psittacine birds such as parrots, macaws, parakeets. However, non-psittacine birds including pigeons, doves and mynah birds can also harbour the infectious agent (Greco, Corrente, & Martella, 2005). Therefore, pigeons are thought to be an underestimated source of human chlamydiosis. Studies have shown that pigeons pose a substantial zoonotic risk as are often shown to be naturally infected with a number of viruses, bacteria, fungi and protozoa that are pathogenic to humans. The potential for zoonotic infection is increased as these birds live in close contact with human beings. The aim of this overview is to present the zoonotic potential of C. psittaci in infected feral pigeon populations, in the context of its history, epidemiology and current approaches in treatment and prevention.
Pigeon population in urban areas
Commonly known as ‘urban’, ‘street’ or ‘city’ pigeons, the feral rock dove (C. livia) is an abundant bird species that often thrive in streets, squares and parks where they come into close contact with humans. Pigeon populations in most large cities increased worldwide after World War II. They have made contributions of considerable importance to humanity, especially in times of war. Feral pigeons have been domesticated and were put to use by making them messengers due to their homing abilities (Dickx et al., 2010). Pigeons are one of the few animal species able to survive in our noisy and hectic cities. They are extremely adaptable, which also enables them to accept breeding places that are unnatural to them, e.g. on trees or over running ventilation systems (Magnino et al, 2009). They are also a valuable enrichment to the urban environment as they have a cleaning up function by eating discarded food. In addition, they may represent as a tourist attraction as feeding and care of feral pigeons may be rewarding spare-time activities for many people who enjoy the company of animals (Magnino et al, 2009). The extensive food supply and minimal predator population has indeed provided the ecological basis for the large populations that occur in most cities of the world.
Chlamydophila psittaci in pigeons
The increase of feral pigeon populations in many cities is a major cause of concern as they are a source of a large number of zoonotic agents. The most important pathogenic organism transmissible from feral pigeons to humans is Chlamydophila psittaci. In fact, studies in Europe have shown as high as 95.6% seropositivity values for C.psittaci in feral pigeon populations (Magnino et al., 2009). C. psittaci an obligate intracellular bacterium causes avian chlamydiosis in birds and psittacosis in humans. The bacterium is commonly recognised in psittacine birds such as parrots, macaws, cockatoos and parakeets. It is also indentified in non-psittacine birds such as pigeons, doves and mynah birds (Greco, Corrente, & Martella, 2005). There are at least six distinct serovars (A to F) of C. psittaci considered endemic in birds (Seth-Smith et al., 2011). Each serovar appears to be associated, though not exclusively, with a different group or order of birds, from which it is most commonly isolated. Genotype B is the most prevalent in pigeons, but the more virulent genotypes A and D have also been discovered (Seth-Smith et al., 2011). All serovars should be considered to be readily transmissible to humans. The avian strains can infect humans and other mammals, and may cause severe disease and even death. In contrast to the devastating explosive outbreaks in the first half of the 20th century, the present outbreaks are characterized by respiratory signs and low mortality (Harkinezhad, Geens & Vanrompay, 2009).
Chlamydophila psittaci has been demonstrated in about 465 bird species comprising 30 different bird orders (Greco, Corrente, & Martella, 2005). The highest infection rates are found in psittacine birds and pigeons. The first case of C. psittaci zoonotic transmission from pigeons was described in 1941. A mother and her daughter had picked up a sick feral pigeon in the street in New York City. The pigeon died after four days and, two weeks later, both mother and daughter developed psittacosis with fever and pneumonia (Dickx et al., 2010). Since then, 47 zoonotic cases linked to pigeons have been reported (Dickx et al., 2010). As a consequence, feral pigeon populations have been repeatedly blamed as vectors for the transmission of C. psittaci infections to humans. Caution is needed, as zoonotic transmission from feral pigeons is known to be an underestimated source of infection.
Psittacosis in birds
Transmission of C. psittaci primarily occurs from one infected bird to another susceptible bird in close proximity. The agent is usually excreted in faeces and nasal discharges. From time to time, faecal shedding occurs and can be activated through stress caused by nutritional deficiencies, prolonged transport, overcrowding, chilling, breeding, egg laying, treatment or handling (Vanrompay et al., 2007). Bacterial excretion periods during natural infection can vary depending on virulence of the strain, infection dose and host immune status. The most common routes of transmission of C. psittaci in nature are the inhalation and ingestion of contaminated material and, sometimes, ingestion (Vanrompay et al., 2007). The bacterium can be also transmitted in the nest. In many species, such as columbiformes, transmission from parent to young may occur through feeding, by regurgitation, while the contamination of the nesting site with infective faeces are also important sources of infection (Vazquez et al., 2010). Also the transmission of C. psittaci may also be facilitated by arthropod vectors in the nest environment, but its occurrence has not been assessed in the wild. Vertical transmission has been demonstrated in other types of avian species. However, occurrence appears to be fairly low.
Chlamydiosis is a common chronic infection of pigeons. C. psittaci infection may result in lethargy, anorexia, ruffled feathers, ocular and nasal discharge, conjunctivitis, diarrhea and excretion of green to yellow urates (West, 2011). Most infected feral pigeons are asymptomatic and latent carriers of C. psittaci, which makes it difficult to assess the risk of transmission of the bacterium to other animals, including humans. As mentioned earlier, increased shedding of the infectious agents may be triggered by stress factors such as other concurrent infections or infestations, lack of food, breeding and overcrowding. It is important to note that as the density of nesting and roosting pigeons increases, the quality of life in the feral pigeon population deteriorates (Dickx et al., 2010). In fact, excessive population density activates and stimulates regulation mechanisms that decimate nestlings and juvenile pigeons with infectious and parasitic diseases (Hedemma et al., 2006). Crowded breeding places make pigeons behave more aggressively, which again mostly affects nestlings and juveniles that are the weakest members of the population, leading to a progressive spoiling of their physical condition. Thus, it is important for feral pigeon populations to be managed carefully in the urban environment to obtain an appropriate- sized and healthy population.
Psittacosis in humans
Although psittacine birds are the major source of human infection, outbreaks due to exposure to non-psittacine birds may also occur. The more common of these are due to exposure to pigeons, both wild and domestic. Humans most often become infected by inhaling the organism when urine, respiratory secretions or dried faeces of infected birds are dispersed in the air as very fine droplets or dust particles (Smith et al., 2011). Other sources of exposure include mouth-to-beak contact, a bite from an infected bird or handling the plumage and tissues of infected birds (Smith et al., 2011). A study by Smith et al. (2011) suggests that more than half of the human cases were due to exposure to C.psittaci through contaminated dust, direct contact with pigeons through feeding and handling pigeons. In addition, about 40 of the cases resulted from transient contacts with feral pigeons such as eating lunch in a park frequented by pigeons, walking through a pigeon flock, and living in a neighbourhood frequented by pigeons (Vazquez et al., 2010). The disease in humans varies from a flu-like syndrome to a severe systemic disease with pneumonia and possibly encephalitis. The disease is rarely fatal in patients treated promptly and correctly. The incubation period is usually 5–14 days, but longer incubation periods are known (Smith et al., 2011). Common symptoms of infection in humans include headache, chills, malaise and myalgia, with or without signs of respiratory involvement (Smith et al., 2011). Therefore, awareness of the danger and early diagnosis are important. Transmission of psittacosis from human to human is rare but can occur. Transmission from humans to birds has not been documented.
Diagnoses
The diagnosis of C. psittaci infections in birds can be a problem because of the occurrence of persistent infections in non-shedding clinically healthy birds. Isolation of C.psittaci is currently regarded as the standard method for the determination of active infections of birds. Polymerase chain reaction (PCR) techniques have been also used to detect C. psittaci in samples of tissues, feces and respiratory specimens, and were found to be quite sensitive and rapid. Diagnoses can also be established by clinical presentation and positive antibodies against C. psittaci using microimmunoflourescence (MIF) methods (Seth-Smith et al., 2011). Conventional ELISA tests have been developed for detecting antibodies to C. psittaci in birds, however, it tends to sensitivity and specificity.
Treatment
No commercial vaccine is available for avian chlamydiosis. Antibiotic treatment of birds is the usual response to known infections. Tetracyclines are usually considered the drugs of choice although quinolones or macrolides have also been used (Tully, 2001). Chlortetracycline (CTC) is given on food depending on the bird species to be treated and type of food (Tully, 2001). Another drug that has also proved to be effective is doxycycline, which has been used for injecting and to treat bird food/ drinking water.
Tetracycline antibiotics are the drug of choice for C.psittaci infection in humans. Mild to moderate cases can be treated with oral doxycycline or tetracycline hydrochloride (West, 2011). Severely ill patients should be treated with intravenous (IV) doxycycline hyclate. Treatment with antimicrobial drugs in humans usually lasts for 3 weeks while birds are treated for 45 days. Most C.psittaci infections are responsive to antibiotics within 1 to 2 days, however relapses can occur (Seth-Smith et al., 2011). Therefore sensible use of these drugs is very important, to prevent the development of drug-resistant bacterial strains
Prevention
Management of feral pigeon populations in the urban environment is a complex issue that requires careful planning. Education initiatives to communicate the health risks and recommendations for minimizing these risks should primarily be directed at susceptible groups such as the elderly, young children, immunosupressed individuals, homeless, and occupationally exposed groups (Harkinezhad, Geens & Vanrompay, 2009). Children should be warned not to handle sick or dead pigeons and immunocompromised individuals should be educated to carefully limit their contact with feral pigeons. Strict hygienic procedures should also be enforced when dealing with birds. Pigeon feeders should be encouraged to stop or limit their activity by implementing a feeding ban in defined urban areas (Harkinezhad, Geens & Vanrompay, 2009). Furthermore, preservation of urban hygiene is very important and should be included in the aims of administrators and health officials, as it will lead to a reduced and healthier feral pigeon population (Vazquez et al., 2010). The relationship between feeding, overcrowding, and the deterioration of living conditions of pigeons, should be the main focus when educating the general public.
Monitoring for C. psittaci infections over time, by direct detection of the organism and/or by specific antibody testing, should also be considered in those who are in frequent close contact with bird puplations (ie. occupationally exposed workers) (Smith et al., 2011). In addition, preventive measures such as wearing protective clothes with hoods, boots, gloves and air filter face masks should be worn when removing pigeon faeces from roofs, attics and/or buildings. Finally, for the sake of animal protection, visibly sick birds should be captured and taken into veterinary care where they should be appropriately treated with effective drugs such as tetracyclines, quinolones or macrolides (Seth-Smith et al., 2011). .
Conclusion
Feral pigeons, more commonly known as ‘urban’ or ‘city’ pigeons, are present in both urban and rural areas all over the world. Due to frequent and close contact with people, pigeons are a public health concern as they are a source of many zoonotic agents. In particular Chlamydophila psittaci, a bacterium known to cause psittacosis in both birds and humans (Harkinezhad, Geens & Vanrompay, 2009). Due to the growing population of pigeons, contact with infected pigeons or pathogen transmission is greatly increased. The infectious agent can be easily transmitted to humans through inhalation of contaminated dust and aerosols from infected pigeons or their feces. Once infected, people suffer from various conditions including mild influenza-like symptoms or severe pneumonia.
In addition, the huge increase of feral pigeon populations in many cities is a major cause of concern due to the detrimental effect of pigeon droppings on environmental hygiene. Therefore it is important to monitor the health of both city bird populations and humans who come in close contact with possibly infected birds. As well, awareness and preventative measures must be taken into consideration when handling infected birds or their feces. Furthermore, management of feral population and preservation of urban hygiene is very important in controlling psittacosis.

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