A Probable Mechanism for Recurring Outbreak of Respiratory Syndrome During Autumn Season in Ahvaz City, Iran

Document Type : Original Article


Department of Biology, Faculty of Science, Shahid Chamran University of Ahvaz, Ahvaz, Iran.



Background: Recurring annual asthma or asthma-like outbreak in Ahvaz City, Iran, has become a serious public health problem. A toxic gas, a chemical compound, or an allergen with unknown nature and mechanism leads to severe asthma outbreaks each year. Bronchospasm, cough, dyspnea, chest tightness, and wheezing are the main symptoms of these attacks. Oxygen and anti-asthma therapy are effective treatments in outbreak management. Based on our findings, it is hypothesized that vast amounts of ammonium nitrate used in agriculture underlay high concentrations of nitrate. This substance is transported by PM10 and is the main cause of the respiratory outbreak.
Methods: The concentration of nitrate was determined by the ion chromatography method in dust samples during 2015-2016. Using spectroscopic methods, the effect of nitrate ions on hemoglobin oxidation and methemoglobin formation was studied.
Results: Our results indicate that the concentration of ammonium nitrate in dust collected from indoor spaces is five times higher than the levels allowed amount in airborne pollutants. Our findings also indicate that this concentration of nitrate in the bloodstream can instantly increase methemoglobin percent to 18% with symptomatic consequences.
Conclusion: The exact mechanism proposed by this study is that inhaled nitrate or nitric acid finally increases the nitrate in the circulation of affected individuals. Hemoglobin oxidation and methemoglobin formation are the subsequent events leading to methemoglobinemia with asthma-like reactions seen in Ahvaz respiratory syndrome. Restricting or even prohibiting ammonium nitrate application in agriculture seems to be an urgent measure to stop Ahvaz's recurring respiratory syndrome.


  1. Forouzan A, Masoumi K, Haddadzadeh Shoushtari M, Idani E, Tirandaz F, Feli M, et al. An overview of thunderstorm-associated asthma outbreak in southwest of Iran. J Environ Public Health. 2014; 2014:504017. [DOI:10.1155/2014/504017] [PMID] [PMCID]
  2. Dabrera G, Murray V, Emberlin J, Ayres JG, Collier C, Clewlow Y, et al. Thunderstorm asthma: an overview of the evidence base and implications for public health advice. QJM. 2013; 106(3):207-17. [DOI:10.1093/qjmed/hcs234] [PMID]
  3. Hassanvand MS, Naddafi K, Faridi S, Arhami M, Nabizadeh R, Sowlat MH, et al. Indoor/outdoor relationships of PM10, PM2.5, and PM1 mass concentrations and their water-soluble ions in a retirement home and a school dormitory. Atmos Enviro. 2014; 82:375-82 [DOI:10.1016/j.atmosenv.2013.10.048]
  4. Idani E, Raji H, Madadizadeh F, Cheraghian B, Haddadzadeh Shoshtari M, Dastoorpoor M. Prevalence of asthma and other allergic conditions in adults in Khuzestan, southwest Iran, 2018. BMC Public Health. 2019; 19:303 [DOI:10.1186/s12889-019-6491-0] [PMID] [PMCID]
  5. Carrillo G, Patron MJP, Johnson N, Zhong Y, Lucio R, Xu X. Asthma prevalence and school-related hazardous air pollutants in the US-Mexico border area. Environ Res. 2018; 162:41-8. [DOI:10.1016/j.envres.2017.11.057] [PMID]
  6. Heidari-Farsani M, Shirmardi M, Goudarzi G, Bakhtiarivand NA, Ahmadi-Ankali K, Zallaghi E, et al. The evaluation of heavy metals concentration related to PM10 in ambient air of Ahvaz city, Iran. J Adv Environ Health Res. 2013; 1(2):120-8. [doi: 10.22102/jaehr.2013.40133]
  7. Bagheri A. A descriptive study on how to control, prevent and combat pollutant factors (A case study, Ahvaz city in Khuzestan province, Iran). Int Res J Appl Basic Sci. 2015; 9(3):262-7. https://irjabs.com/files_site/paperlist/r_2511_150227144926.pdf
  8. Arvin AA, Rahimi M, Qoli MA. Deadly Tsunami and the negative impact on Iran border regions (Case study: Ahvaz, Iran). J NovAppl Sci. 2014; 3(7):719-23. http://jnasci.org/wp-content/uploads/2014/07/719-723.pdf
  9. Bahrami F, Kermani M, Aghaei M, Karimzadeh S, Salahshour Arian S, Shahsavani A, et al. [Estimation of diseases and mortality attributed to NO2 pollutant in five metropolises of Iran using Air Q model in 2011-2012 (Persian)]. J Mazandaran Univ Med Sci. 2015; 24(121):239-49. http://eprints.iums.ac.ir/5773/
  10. Parvizimehr A, Norouzian Baghani A, Hoseini M, Sorooshian A, Cuevas-Robles A, et al. On the nature of heavy metals in PM10 for an urban desert city in the Middle East: Shiraz, Iran. Microchem J. 2020; 154:104596. [DOI:10.1016/j.microc.2020.104596]
  11. Zallaghi E, Goudarzi G, Geravandi S, Mohammadi MJ. Epidemiological indexes attributed to particulates with less than 10 micrometers in the air of Ahvaz city during 2010 to 2013. Health Scope. 2014; 3(4):e22276 [DOI:10.17795/jhealthscope-22276]
  12. Goudarzi G, Geravandi S, Mohammadi MJ, Vosoughi M, Ahmadi Angali K, Zallaghi E, et al. Total number of deaths and respiratory mortality attributed to particulate matter (PM10) in Ahvaz, Iran during 2009. Int J Env Health Eng. 2015; 4(1):33. [DOI: 10.4103/2277-9183.163978]
  13. Sawyer K, Mundandhara S, Ghio AJ, Madden MC. The effects of ambient particulate matter on human alveolar macrophage oxidative and inflammatory responses. J Toxicol Environ Health A. 2010; 73(1):41-57 [DOI:10.1080/15287390903248901] [PMID]
  14. Snow SJ, De Vizcaya-Ruiz A, Osmomio-Vargas A, Thomas RF, Schladweiler MC, McGee J, et al. The effect of composition, size, and solubility on acute pulmonary injury in rats following exposure to mexico city ambient particulate matter samples. J Toxicol Environ Health A. 2014; 77(19):1164-82. [DOI:10.1080/15287394.2014.917445] [PMID]
  15. Tsai SS, Yang CY. Fine particulate air pollution and hospital admissions for pneumonia in a Subtropical City: Taipei, Taiwan. J Toxicol Environ Health A. 2014; 77(4):192-201. [DOI:10.1080/15287394.2013.853337] [PMID]
  16. Gerivani H, Lashkaripour GR, Ghafoori M, Jalali N. [The source of dust storm in Iran: A case study based on geological information and rainfall data (Persian)]. Carpath J Earth Env. 2011; 6(1):297-308. https://profdoc.um.ac.ir/paper-abstract-1019133.html
  17. Ashrafi K, Shafiepour-Motlagh M, Aslemand A, Ghader S. Dust storm simulation over Iran using HYSPLIT. J Environ Health Sci Eng. 2014; 12:9. [DOI:10.1186/2052-336X-12-9] [PMID] [PMCID]
  18. Draxler RR, Gillette DA, Kirkpatrick JS, Heller J. Estimating PM10 air concentrations from dust storms in Iraq, Kuwait and Saudi Arabia. Atmos Environ. 2001; 35(25):4315-30. [DOI:10.1016/S1352-2310(01)00159-5]
  19. Goudie AS, Middleton NJ. Saharan dust storms: nature and consequences. Earth Sci Rev. 2001; 56(1-4):179-204. [DOI:10.1016/S0012-8252(01)00067-8]
  20. Leon JF, Legrand M. Mineral dust sources in the surroundings of the North Indian Ocean. Geophys Res Lett. 2003; 30(6). [DOI:10.1029/2002GL016690]
  21. Pope CA 3rd, Dockery DW. Health effects of fine particulate air pollution: lines that connect. J Air Waste Manag Assoc. 2006; 56(6):709-42. [DOI:10.1080/10473289.2006.10464485] [PMID]
  22. Geravandia S, Goudarzic G, Vosoughid M, Salmanzadehe S, Mohammadib MJ, Zallaghif E. Determination of behavior particulate matter less than 10 microns and effects on human health in Ahvaz, Southwest Iran. Arch Hyg Sci. 2015; 4(2):64-72. http://jhygiene.muq.ac.ir/article-1-41-en.html
  23. Idani E, Dastoorpoor M, Goudarzi G, Khanjani N. Severe outbreaks of respiratory syndromes following autumn rainfall in Khuzestan. Arch Iran med. 2016; 19(12):884-5. [PMID]
  24. Mirhosseini SH, Birjandi M, Zare MR, Fatehizadeh A. Analysis of particulate matter (PM10and PM2.5) concentration in Khorramabad city. Int J Env Health Eng. 2013; 2:3. [DOI:10.4103/2277-9183.106635]
  25. Bauer SE, Koch D, Unger N, Metzger SM, Shindell DT, Streets DG. Nitrate aerosols today and in 2030: a global simulation including aerosols and tropospheric ozone. Atmos Chem Phys. 2007; 7(2):5553-93 [DOI:10.5194/acp-7-5043-2007]
  26. Rezaei M, Salimi A, Taghidust M, Naserzadeh P, Goudarzi G, Seydi E, et al. A comparison of toxicity mechanisms of dust storm particles collected in the southwest of Iran on lung and skin using isolated mitochondria. J Toxicol Environ Chem. 2014; 96(5):814-30. [DOI:10.1080/02772248.2014.959317]
  27. Kleinman MT, Linn WS, Michael RM, Jones P, Hackney JD. Effect of Ammonium Nitrate Aerosol on human respiratory function and symptoms. Environ Res. 1980, 21(2):317-26 [DOI:10.1016/0013-9351(80)90033-X]
  28. Larson TV, Taylor GS. On the evaporation of ammonium nitrate aerosol. Atmos Environ. 1983; 17(12):2489-95. [DOI:10.1016/0004-6981(83)90074-4]
  29. Goudarzi G, Mohammadi MJ, Ahmadi Angali K, Neisi AK, Babaei AA, Mohammadi B, et al. [Estimation of health effects attributed to NO2 exposure using airQ model (Persian)]. Arch Hyg Sci. 2012; 1(2):59-66. https://www.sid.ir/en/Journal/ViewPaper.aspx?ID=307374
  30. Shahsavani 30 A, Naddafi K, Jaafarzadeh Haghighifard N, Mesdaghinia A, Yunesian M, Nabizadeh R, et al. Characterization of ionic composition of TSP and PM10 during the Middle Eastern Dust (MED) storms in Ahvaz, Iran. Environ Monit Assess. 2012; 184(11):6683-92. [DOI:10.1007/s10661-011-2451-6] [PMID]
  31. Shahsavani 31 A, Naddafi K, Jafarzade Haghighifard N, Mesdaghinia A, Yunesian M, Nabizadeh R, et al. The evaluation of PM10, PM2.5, and PM1 concentrations during the Middle Eastern Dust (MED) events in Ahvaz, Iran, from april through september 2010. J Arid Environ. 2012; 77:72-83 [DOI:10.1016/j.jaridenv.2011.09.007]
  32. Kohn MC, Melnick RL, Ye F, Portier CJ. Pharmacokinetics of sodium nitrite-induced methemoglobinemia in the rat. Drug Metab Dispos. 2002; 30(6):676-83. [DOI:10.1124/dmd.30.6.676] [PMID]
  33. Chitsazan M, Faryabi M, Zarasvandi A, Negarestani A. Evaluation of the spatio-temporal variability in river and groundwater interactions, an example from South West of Iran. Int J Sci Res Environ Sci 2015; 3(4):147-58 [DOI:10.12983/ijsres-2015-p0147-0158]
  34. Shihana F, Dissanayake DM, Buckley NA, Dawson AH. A simple quantitative bedside test to determine methemoglobin. Ann Emerg Med. 2010; 55(2):184-9 [DOI:10.1016/j.annemergmed.2009.07.022] [PMID] [PMCID]
  35. Gorguner M, Akgun M. Acute inhalation injury. Eurasian J Med. 2010; 42(1):28-35 [DOI:10.5152/eajm.2010.09] [PMID] [PMCID]
  36. Soleimani N, Faridnouri H, Dayer MR . The effect of dusts on liver enzymes and kidney parameters of serum in male rats in Khuzestan, Iran. J Chem Health Risks. 2020; 10(4):315-26. [doi: 10.22034/jchr.2020.1902789.1148]
  37. Chitsazan M, Rezapour Tabari MM, Eilbeigi M. Analysis of temporal and spatial variations in groundwater nitrate and development of its pollution plume: a case study in Karaj aquifer. Environ Earth Sci. 2017; 76:391 [DOI:10.1007/s12665-017-6677-7]
  38. Dayer MR, Moosavi-Movahedi AA, Dayer MS. Band assignment in Hemoglobin porphyrin ring spectrum: Using four-orbital model of gouterman. Protein Pept Lett. 2010; 17(4):473-9 [DOI:10.2174/092986610790963645] [PMID]
  39. Whitehead Jr RD, Mei Z, Mapango C, Jefferds MED. Methods and analyzers for hemoglobin measurement in clinical laboratories and field settings. Ann N Y Acad Sci. 2019; 1450(1), 147-71. [DOI:10.1111/nyas.14124] [PMID] [PMCID]
  40. Ward MH, Jones RR, Brender JD, de Kok TM, Weyer PJ, Nolan BT, et al. Drinking water nitrate and human health: An updated review. Int J Environ Res Public Health. 2018; 15(7):1557. [DOI:10.3390/ijerph15071557] [PMID] [PMCID]
  41. Alavi SM, Bakhtiyariniya P, Eghtesad M, Salmanzadeh S. Prevalence of pulmonary tuberculosis before and after soil dust in Khuzestan, South West Iran. Caspian J Intern Med. 2014; 5(4):190-5. [PMCID]
  42. Goudarzi G, Zallaghi E, Neissi A, Ahmadi Ankali K, Saki A, Babaei AA, et al. [Cardiopulmonary mortalities and chronic obstructive pulmonary disease attributed to ozone air pollution (Persian)]. Arch Hyg Sci. 2013; 2(2):62-72. https://www.sid.ir/en/journal/ViewPaper.aspx?id=438584
  43. Goudarzi G, Geravandi S, Foruozandeh H, Babaei AA, Alavi N, Vosoughi Niri M, et al. Cardiovascular and respiratory mortality attributed to ground-level ozone in Ahvaz Iran. Environ Monit Assess. 2015; 187(8):487 [DOI:10.1007/s10661-015-4674-4] [PMID]
  44. Goudarzi G, Geravandi S, Naimabadi A, Mohammadi MJ, Neisi AK, Taghavirad SS, et al. Cardiovascular deaths related to Carbon monoxide Exposure in Ahvaz, Iran. Iran J Health Saf Environ. 2014; 1(3):126-31. http://www.ijhse.ir/index.php/IJHSE/article/view/50
  45. Soleimani Z, Parhizgari N, Dehdari Rad H, Akhoond MR, Kermani M, Bagherian Marzouni M, et al. Normal and dusty days comparison of culturable indoor airborne bacteria in Ahvaz, Iran. Aerobiologia. 2015; 31:127-41 [DOI:10.1007/s10453-014-9352-4]