Archives of

1. Introduction
Acute avian influenza (AI) occurs in animal populations, especially poultry, and can be transmitted to humans. Therefore, not only does the virus infect humans and cause severe disease with a high mortality rate, but also it has the ability to adapt to humans. As a potential pathogen for humans or in combination with other human influenza viruses, AI gives rise to a pathogen capable of causing a pandemic [1–3]. Among the necessary measures to control this infection, implementing the environmental surveillance system program, which is a regular and continuous process of collecting data related to diseases, analyzing them with the aim of determining the disease status, and implementing appropriate measures to control the infection based on epidemiological indicators are inevitable [4–6]. Spatial analysis has become highly important in the control of human and animal diseases in surveillance systems [7–9]. Given the prevalence of this disease around the world and the impact of various environmental risk factors on the incidence of this disease, the use of spatial modeling in identifying high-risk sites of this disease can be effective in implementing control and prevention programs. Clustering and spatial spread of AI outbreaks may provide clues as to the causes of infection that are effective in disease control and prevention programs [10–13]. In a recent survey conducted on the subject of AI, environmental risk factors have been reported to have a highly important role in the spread of the infection. In their study about the prevalence and risk factors for the AI virus in Bangladesh, Islam et al found that disposal of waste, cleaning and disinfectant agents, access of dogs, and inadequate biosecurity measures have increased the risk of AI transmission in Bangladesh [14]. The latest findings on the subject strategies to manage an outbreak of avian flu pathogens in 2023 revealed that for approved confirmed case, containment and prevention actions must be in the infected poultry cases or infected materials. The prevention measures for confirmed cases include the sanitary slaughter of infected poultry, environmental disposal, and incineration and disinfection of affected poultry farms [15]. Accordingly, considering the existence of about 600 poultry breeding units in Qom province in the central part of Iran and the density and proximity of poultry farms to each other, as well as the specific environmental factors of Qom province (e.g., climate conditions and social and cultural infrastructure), it seems that it is one of the important factors in the spread of the disease [16,17]. Accordingly, this study sought to
evaluate the environmental risk factors in the outbreak of
AI infection in Qom province to provide essential data for
developing effective interventions in infection control.
2. Materials and Methods
2.1. Study Setting
Qom, the capital of Qom province, is located on the
boundary of the central desert of Iran (Kavir Markazi) with
geographical attributes of 34°38′24″N and 50°52′35″E.
At the 2017 census, the population of this province was
1 200 000. In this study, the cross-sectional method was
predicted and implemented in two specific phases from
the end of 2018 to 2019 in all parts of the province. In
the primary phase of the study, the required criteria
were extracted by applying a questionnaire and standard
checklists (questionnaire of control and environmental
care of poultry farm units to control AI taken from the
Center for Disease Management of the Ministry of Health
in Iran). The reliability and validity of the questionnaire
were evaluated and confirmed. Table 1 presents some
of the main questions summarized in five sections. All
poultry farms in the province that are registered in the
Disease Monitoring and Care Information System of the
Iran Veterinary Organization by means of a questionnaire
have been evaluated in this study.
In this study, a stratified sampling method was
performed based on the ratio of poultry breeding units
in the districts of Qom province. The number of samples
required for sampling (n = 175) was calculated based on
the prevalence rate of 50%, accuracy of 5%, and a 95%
confidence level (Figure 1). In another part of the study,
the characteristics and spread of the infection in Qom
province, including location, type and number of birds,
longitude, latitude, and longitude, and other required
data, were determined using DotMapper software based
on the geographic information system, which is usually
used to distribute the disease display [18].
2.2. Statistical Analysis
The relationship between outbreak occurrence and
environmental risk factors was determined by logistic
regression models and odds ratios (ORs) using GraphPad
Prism software (2019).
3. Results
The results of the study are provided based on the
method described in Tables 2–3 and Figures 1–3.
Tables 2 and 3 present the characteristics of poultry farms,
outbreak cases, and evaluation of environmental risk
factors for avian influenza in the outbreak of influenza
Table 1. Summarized Questionnaire of Environmental Risk Factors in the Outbreak of Avian Influenza Infection in Poultry Farm Units
No. Preparedness to Respond to Environmental Emergencies Before the Occurrence of the Infection
1
Have factors that cause the “indigenization” of disease in birds in a region, including the quality of the disease care system in birds, the movement of
birds according to the necessity of biosecurity through trade or smuggling, or migration of birds, been visited and evaluated?
2
Have all the necessary materials and equipment, especially personal protective equipment such as general clothing, special masks, eye protection
equipment, gloves, and rubber boots (or plastic covering for shoes) been prepared in advance?
3 Is the provision of effective disinfectants planned and stored in the right place?
4 Is there a trained manpower to form a special extermination team in the unit?
Evaluation of Measures Taken at the Time of Infection
5
Have complete quarantine and prohibition of leaving the poultry unit without the permission of the veterinarian and extermination team been
performed?
6 Has the entry of different people been prohibited at the bird farm?
7
Has the sign of the area infected with the avian influenza virus been installed in confirmed cases at a distance between 500 and 100 meters from the
road leading to the poultry farm?
8
Have infected flock birds, waste, and consumables in the bird farm area and at a depth of at least 3 meters above the ground level and at least one
meter above the underground water level been exterminated and destroyed?
9
Has the movement of birds been controlled in the protected area (with a radius of at least 3 kilometers) and the monitoring area (with a radius of at
least 10 kilometers) around the contaminated area?
10
Have all materials that cannot be disinfected, such as dead birds, eggs, bedding, manure, fresh and frozen carcasses, as well as tools and equipment,
been effectively and immediately destructed after placing them in impermeable plastic bags?
11 Are composted litter and manure protected for at least 60 days and buried carcasses for at least 4 months?
12
Have the poultry hall and the use of effective disinfectants in the form of aerosols, especially for the disinfection of ventilators, disinfection of poultry
vehicles, equipment, and disinfection of worker houses, poultry offices, and the like, been decontaminated?
13
Is the preparation of minutes of the meeting and the preservation of documents related to the extermination and disposal of the carcass and its waste
completely archived and preserved?
Evaluation of Environmental Health Facilities
14 Are the facilities for the sanitary disposal of manure and waste in poultry breeding centers suitable?
15 Are the employees’ health facilities, including toilets, bathrooms, lockers, and staff lockers, in suitable conditions?
16 Is the source of supply, including a well, a water storage tank, and the quality of the used water, approved?
17 Is the power and capacity of ventilation of the poultry unit suitable and capable of moving air at a rate of 10 times per hour?
Arch Hyg Sci. Volume 12, Number 4, 2023 189
Environmental risk factors in the outbreak of avian influenza infection
infection in poultry farm units in the studied regions and
districts in Qom province. Figures 2 and 3 display the
geographic distribution, spread, and distribution map of
AI based on control of environmental risk factors.
4. Discussion
According to the results (Table 2) regarding the
characteristics of poultry farms, outbreak cases, and
environmental risk factors, from a total of 128 investigated
farms, 95 farm units (%54) were infected and were positive
for AI. In the evaluation of how to manage environmental
health risk factors, the results showed that at least one of
the environmental risk factors was not controlled in 86%
of laying poultry farms and 66% of broiler poultry farms,
according to the questionnaire. The findings (Figure 3)
demonstrated that, despite the control of environmental
risk factors, the density and proximity of poultry units
played a significant role in the spread of infection. Based
on the findings of statistical analyses (Table 3), sanitary
land disposal of infected poultry carcasses, waste and
manure of birds (OR = 1.02), and complete quarantine
and installation of warning signs in contaminated areas
(OR = 0.55) were related to AI infection on poultry farms
in Qom province. In addition, the existence of facilities
and performance decontamination and the use of
Figure 1. Location of the Study Area effective disinfectants for the disinfection of ventilators,
Table 2. Characteristics of Poultry Farms, Outbreak Cases, and Environmental Risk Factors
Poultry Farm Type
Sum of Investigated
Farms
Number of Infected
Farms
The Number of Farms That Have Not Managed Environmental Risk
Factors According to the Questionnaire in at Least One Case
Laying poultry farm 73 34 29 (86%)
Broiler poultry farm 78 41 27 (66%)
Turkey poultry farm 6 5 3 (60%)
Hen poultry farm 5 4 3 (75%)
Ornamental poultry farm 6 5 3 (60%)
Quail poultry farm 4 3 2 (66%)
Duck poultry farm 3 3 3 (100%)
Table 3. Evaluation of Environmental Risk Factor Affecting of Avian Influenza Infection in Poultry Farm Units
Environmental Risk Factors Odds Ratio P Value
Preparedness and existence of a response plan to environmental emergencies for avian influenza infection 0.018 < 0.001
Complete quarantine and installation of warning signs in contaminated areas at a distance of 500 and 100 meters from the road
leading to the poultry farm
0.55 < 0.05
Sanitary land disposal of infected poultry carcasses, waste, and manure of birds at a depth of at least 3 meters above the ground
level
1.02 0.033
Existence of facilities and performance decontamination and the use of effective disinfectants for the disinfection of ventilators,
disinfection of poultry vehicles, equipment, and manure of bird
0.33 < 0.05
Existence of suitable facilities, including toilets, bathrooms, and lockers for employees 0.21 0.061
Approval of the water supply system, water storage tank, and microbial quality of the water 0.16 0.042
Approval of power and capacity of ventilation of the poultry unit for moving displacement of air at the rate of 10 times per hour 0.044 0.022
Ghafuri et al
190 Arch Hyg Sci. Volume 12, Number 4, 2023
disinfection of poultry vehicles, equipment, and manure
of birds (OR = 0.33) had a noticeable association with AI
infection on poultry farms in this province. The results
of the present study are important in comparison with
those of studies evaluating environmental risk factors and
outbreaks of AI. The findings of the study by Fang et al
regarding the environmental factors and spread of H5N1
AI in mainland China indicated that environmental
factors, including minimal distance to the nearest national
highway, rate of annual precipitation, and the interaction
between minimal distance to the nearest lake and wetland,
are related to the spread of the infection [19]. Although the
environmental variables and risk factors evaluated in the
above-mentioned study contradict those of the present
study, it should be noted that in both studies, attention
has been paid to the role of environmental factors in
the spread of infection. The results of a survey on the
risk factors of AI on poultry farms in the meta-analysis
study by Wang et al demonstrated that unsanitary water
sources, infections on nearby farms, other livestock, and
disinfection of farms have a significant association with
AI infection on poultry farms [20]. The results of this
study are in line with those of the present study. Based
on the results of a predictive risk analysis for occurrences
of AI (H5N1) by Si et al in wild birds in Europe, H5N1
occurrences were influenced by the availability of food
resources, an increase in temperatures, and a decrease in
precipitation [21]. This study also confirms the results
of the current study with the approach of controlling
environmental factors and improving the environment.
One of the important results of this study is to pay
attention to the issue of sanitation in the outbreak of AI.
In the study of Wang et al, the sanitary condition in the
poultry farms was a protective factor against AI [22],
which is consistent with the results of the present study.
5. Study Limitations
Although environmental risk factors related to AI
prevalence in Qom province were identified, this study
has some limitations. A lack of an accurate environmental
surveillance system for reporting positive cases on poultry
farms in health centers and the lack of high participation
of poultry owners in the interviews and questionnaire
completion are among the limitations of this study.
6. Conclusion
Our findings indicated that control and monitoring
of environmental risk factors as part of an effective
surveillance system for the AI virus are key processes
for the propagation and contribute to the spread of the
infection.
Acknowledgments
This study was financially supported by Qom University of Medical
Science (IR.MUQ.REC.1398.162). We would like to thank the staff
of the Health Center of Qom University of Medical Sciences.
Authors’ Contribution
Conceptualization: Yadollah Ghafuri, Ahmad Reza Yari.
Methodology: Rahim Aali.
Supervision: Yadollah Ghafuri, Ahmad Reza Yari.
Writing–original & draft: Rahim Aali.
Competing Interests
The authors of this article declare that they have no conflict of
interests.
Ethical Approval
This project has been approved by the Qom University
of Medical Sciences Health Services.
Funding
This project has been supported by the Qom University of Medical
Sciences Health Services.
References
1. Simancas-Racines A, Cadena-Ullauri S, Guevara-Ramírez
P, Zambrano AK, Simancas-Racines D. Avian influenza:
strategies to manage an outbreak. Pathogens. 2023;12(4):610.
doi: 10.3390/pathogens12040610 .
2. Chen W, Zhang X, Zhao W, Yang L, Wang Z, Bi H.
Figure 2. Geographic Distribution of Infected Poultry Farm Types in
Districts of Qom Province
Figure 3. Spread and Distribution Map of Avian Influenza According to
Control of Environmental Risk Factors in Poultry Farms in Qom, Iran
Arch Hyg Sci. Volume 12, Number 4, 2023 191
Environmental risk factors in the outbreak of avian influenza infection
Environmental factors and spatiotemporal distribution
characteristics of the global outbreaks of the highly
pathogenic avian influenza H5N1. Environ Sci Pollut Res Int.
2022;29(29):44175-85. doi: 10.1007/s11356-022-19016-1.
3. Alhaji NB, Adeiza AM, Godwin EA, Haruna AE, Aliyu MB,
Odetokun IA. An assessment of the highly pathogenic avian
influenza resurgence at human-poultry-environment interface
in north-central Nigeria: sociocultural determinants and One
Health implications. One Health. 2023;16:100574. doi:
10.1016/j.onehlt.2023.100574.
4. Gooya MM, Soroush M, Mokhtari-Azad T, Haghdoost AA,
Hemati P, Moghadami M, et al. Influenza A (H1N1) pandemic
in Iran: report of first confirmed cases from June to November
2009. Arch Iran Med. 2010;13(2):91-8.
5. Gompo TR, Shah BR, Karki S, Koirala P, Maharjan M, Bhatt
DD. Risk factors associated with Avian Influenza subtype
H9 outbreaks in poultry farms in Kathmandu valley, Nepal.
PLoS One. 2020;15(4):e0223550. doi: 10.1371/journal.
pone.0223550.
6. Li YT, Linster M, Mendenhall IH, Su YCF, Smith GJD. Avian
influenza viruses in humans: lessons from past outbreaks. Br
Med Bull. 2019;132(1):81-95. doi: 10.1093/bmb/ldz036.
7. Huang ML, Wu HD, Chao DY. Approaches for spatial and
temporal-spatial clustering analysis in avian influenza
outbreaks. In: Wen TH, Chuang TW, Tipayamongkholgul M,
eds. Earth Data Analytics for Planetary Health. Singapore:
Springer; 2023. p. 169-84. doi: 10.1007/978-981-19-8765-
6_9.
8. Chen Z, Li K, Luo L, Lu E, Yuan J, Liu H, et al. Detection
of avian influenza A(H7N9) virus from live poultry markets
in Guangzhou, China: a surveillance report. PLoS One.
2014;9(9):e107266. doi: 10.1371/journal.pone.0107266.
9. Fang LQ, Li XL, Liu K, Li YJ, Yao HW, Liang S, et al. Mapping
spread and risk of avian influenza A (H7N9) in China. Sci
Rep. 2013;3:2722. doi: 10.1038/srep02722.
10. Ward MP, Maftei D, Apostu C, Suru A. Environmental and
anthropogenic risk factors for highly pathogenic avian
influenza subtype H5N1 outbreaks in Romania, 2005--2006.
Vet Res Commun. 2008;32(8):627-34. doi: 10.1007/s11259-
008-9064-8.
11. Henning J, Hesterberg UW, Zenal F, Schoonman L, Brum
E, McGrane J. Risk factors for H5 avian influenza virus
prevalence on urban live bird markets in Jakarta, Indonesiaevaluation
of long-term environmental surveillance data.
PLoS One. 2019;14(5):e0216984. doi: 10.1371/journal.
pone.0216984.
12. Liang WS, He YC, Wu HD, Li YT, Shih TH, Kao GS, et al.
Ecological factors associated with persistent circulation
of multiple highly pathogenic avian influenza viruses
among poultry farms in Taiwan during 2015-17. PLoS One.
2020;15(8):e0236581. doi: 10.1371/journal.pone.0236581.
13. Islam K, Ahsan MM, Chakma S, Penjor K, Barua M, Jalal MS, et
al. An assessment on potential risk pathways for the incursion
of highly pathogenic avian influenza virus in backyard poultry
farm in Bangladesh. Vet World. 2020;13(10):2104-11. doi:
10.14202/vetworld.2020.2104-2111.
14. Islam A, Islam S, Islam M, Hossain ME, Munro S, Samad
MA, et al. Prevalence and risk factors for avian influenza
virus (H5 and H9) contamination in peri-urban and rural
live bird markets in Bangladesh. Front Public Health.
2023;11:1148994. doi: 10.3389/fpubh.2023.1148994.
15. EFSA (European Food Safety Authority), ECDC (European
Centre for Disease Prevention and Control), EURL (European
Reference Laboratory forAvian Influenza), Adlhoch C,
Fusaro A, Kuiken T. Avian influenza overview November
2019–February2020. Efsa Journal. 2020;18(3):e06096. doi:
10.2903/j.efsa.2020.6096.
16. Karami Jooshin M, Izanloo H, Saghafipour A, Ghafoori
Y. Study on efficacy of 1% permethrin shampoo and 4%
dimethicone lotion as pediculicide products used in Iran: a
clinical trial. Tehran Univ Med J. 2019;77(1):41-6. [Persian].
17. Saghafipour A, Rassi Y, Abai MR, Oshaghi MA, Farzinnia
B, Mostafavi R, et al. Outbreak of zoonotic cutaneous
leishmaniasis: a report. Arch Hyg Sci. 2013;2(2):48-54.
18. Smith CM, Hayward AC. DotMapper: an open source tool
for creating interactive disease point maps. BMC Infect Dis.
2016;16:145. doi: 10.1186/s12879-016-1475-5.
19. Fang LQ, de Vlas SJ, Liang S, Looman CW, Gong P, Xu
B, et al. Environmental factors contributing to the spread
of H5N1 avian influenza in mainland China. PLoS One.
2008;3(5):e2268. doi: 10.1371/journal.pone.0002268.
20. Wang Y, Li P, Wu Y, Sun X, Yu K, Yu C, et al. The risk
factors for avian influenza on poultry farms: a metaanalysis.
Prev Vet Med. 2014;117(1):1-6. doi: 10.1016/j.
prevetmed.2014.06.008.
21. Si Y, Wang T, Skidmore AK, de Boer WF, Li L, Prins HHT.
Environmental factors influencing the spread of the highly
pathogenic avian influenza H5N1 virus in wild birds in
Europe. Ecol Soc. 2010;15(3):26. doi: 10.5751/es-03622-
150326.
22. Wang XX, Cheng W, Yu Z, Liu SL, Mao HY, Chen EF. Risk
factors for avian influenza virus in backyard poultry flocks and
environments in Zhejiang province, China: a cross-sectional
study. Infect Dis Poverty. 2018;7(1):65. doi: 10.1186/s40249-
018-0445-0.