Archives of Academic Emergency Medicine. 2021; 9(1): e66 REV I EW ART I C L E Aluminum Phosphide Poisoning Mortality Rate in Iran; a Systematic Review and Meta-Analysis Farhad Bagherian1, Navid Kalani2, Fatemeh Rahmanian3, Samaneh Abiri3, Naser Hatami4, Mahdi Foroughian5, Neema John Mehramiz6, Behzad Shahi7∗ 1 Department of Emergency Medicine, Babol University of Medical Sciences, Babol, Iran. 2 Research center for social Determinants of Health, Jahrom University of Medical Sciences, Jahrom, Iran. 3 Department of Emergency Medicine, Jahrom University of Medical Sciences, Jahrom, Iran. 4 Student Research Committee, Jahrom University of Medical Sciences, Jahrom, Iran. 5 Department of Emergency Medicine, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran. 6 Department of Psychiatry Neurology, Banner university medical center, Tucson, AZ, USA. 7 Department of Emergency Medicine, Faculty of Medicine, Zahedan University of Medical Sciences, Zahedan, Iran. Received: September 2021; Accepted: September 2021; Published online: 3 October 2021 Abstract: Introduction: According to statistics provided by the forensic medicine facility of Iran, there are a high num- ber of Aluminum phosphide (ALP) poisoning-related deaths in the country; while the mortality rate varies in different studies. This study aimed to determine a pooled estimate of ALP poisoning mortality rate in Iran. Methods: The present study was a systematic review and meta-analysis of the mortality rate of ALP poisoning in Iran. Through the quarry of Persian and English databases, using “aluminum phosphide”, “phosphine”, “rice pills”, “poisoning”, and “Iran” as keywords, and no time restrictions, studies reporting mortality rate in ALP poi- soning cases were collected. The random-effects model was used to pool the proportions of mortality and age of survivors versus non-survivors. Results: 21 studies with 3432 cases of ALP poisoning were included in this meta-analysis. The pooled mortality rate of ALP poisoning in Iran was 39.6%, (95% CI: 31.5%-47.9%; I2 = 95%). Since there was significant publication bias, the trim-and-fill correction was conducted and the corrected pooled mortality rate was estimated to be 27.3% (95% CI: 18.9%- 36.5%), which is the rate that should be considered for clinical guidance. Morality rate in male and female patients was 62.3% (95% CI: 53.5%-70.8%) and 37.7% (95% CI: 29.2%-46.5%), respectively (p < 0.01). Survivors had significantly lower mean age than non-survivors (SMD: -0.26 (95% CI: -0.37 to -0.15); p < 0.01; I2=0%). Conclusion: According to this report, the Mortality rate of ALP poisoning in Iranian population is about 27%, with men having a higher fatality rate than women. Poisoning at a younger age is associated with better results. Keywords: Aluminum phosphide; Poisoning; phosphine; Mortality; Iran Cite this article as: Bagherian F, Kalani N, Rahmanian F, Abiri S, Hatami N, Foroughian M, John Mehramiz N, Shahi B. Aluminum Phosphide Poisoning Mortality Rate in Iran; a Systematic Review and Meta-Analysis. Arch Acad Emerg Med. 2021; 9(1): e66. https://doi.org/10.22037/aaem.v9i1.1396. 1. Introduction Aluminum phosphide (ALP), known as rice pill in Iran, is a very effective pesticide for commercial and industrial use. The high lethality of ALP is due to phosphine gas (PH3), ∗Corresponding Author: Behzad Shahi; Department of Emergency Medicine, Faculty of Medicine, Zahedan University of Medical Sciences, Zahedan, Iran. Email: mr.shahi87@yahoo.com, Tel: 09151913501, ORCID: http://orcid.org/0000-0001-9884-1542. which is released when ALP reacts with water. The result- ing gas is colorless and has a distinct odor of garlic or rot- ten fish (1). Phosphine gas released in the stomach of in- dividuals who have devoured this pill intentionally or acci- dentally, quickly gets absorbed into body organs and dis- rupts enzymatic activities, causes cell death and disrupts the function of almost all vital organs, namely brain, lungs, and liver (2). Symptoms of poisoning are due to the involvement of the cardiovascular, gastrointestinal, nervous, and pul- monary systems. The most common clinical signs and symp- This open-access article distributed under the terms of the Creative Commons Attribution NonCommercial 3.0 License (CC BY-NC 3.0). Downloaded from: http://journals.sbmu.ac.ir/aaem F. Bagherian et al. 2 toms of ALP poisoning are restlessness, irritability, dizziness, vertigo, tremors, diplopia, imbalance, cough, shortness of breath, abdominal colic, nausea, vomiting, in some cases black vomit, black stools, decreased cardiac output, irreg- ular heartbeat, pulmonary edema, cyanosis, renal impair- ment, jaundice, enlarged liver and spleen, intestinal paral- ysis, seizure, and acute respiratory distress syndrome (1). Se- vere hypotension and shock are the most common symp- toms of severe poisoning (3). Delayed symptoms of intoxica- tion include pulmonary edema, hypocalcemic tetany, cardio- vascular arrhythmia, liver damage, bradycardia, metabolic acidosis, thrombocytopenia, and methemoglobinemia (4). Treatment for ALP poisoning is only supportive treatment, as there is no known antidote available against it. The effective- ness of these treatments in poisoned patients depends en- tirely on the degree of poisoning and the time of arrival at the medical center; the mortality rate following ALP poison- ing varies between different studies. Despite the ban on the public sale of rice pills since 2012, Iran has a high number of ALP poisoning cases (intentional or accidental). According to statistics provided by the forensic medicine facility of Iran, there is a high number of ALP poisoning-related deaths in the country (5). While many observational studies have reported the cases of ALP poisoning; there is no overall view about the mortality rate of ALP poisoning in the country. This study aimed to determine a pooled estimate of the ALP poisoning mortality rate in Iran. 2. Methods 2.1. Study design and setting The present study was conducted based on the preferred reporting items for systematic reviews and meta-analyses (PRISMA) checklist. Scientific sources were searched by two independent researchers from 2000 to 2021. Search for ar- ticles and dissertations in Iranian sources were performed in the University Jihad Scientific Information Center (SID) database, and PubMed / MEDLINE, Scopus, EMBASE, and Web of Science databases with the keywords of “aluminum phosphide”, “phosphine”, “rice pills”, “poisoning”, and “Iran”. English and Persian articles were quarried. The reference list of all articles identified in the early stages was reviewed in or- der to access cited articles that were not found via electronic searches. The studies that reported cases of aluminum phosphide poi- soning in Iran were selected in two stages. First, the ab- stracts of articles obtained in electronic searches were thor- oughly reviewed, and irrelevant or duplicate studies were eliminated. In the second stage, the decision on the final in- clusion of studies was made after reviewing the full text of the studies (Table 1). Information on study characteristics, qual- ity, and results were extracted from each selected article. The criteria for inclusion in the study was to evaluate patients with aluminum phosphide poisoning and present their mor- tality rate. Studies that only looked at the decedents were not included in this study. All articles that met the selection cri- teria were evaluated in terms of methodological quality. The Newcastle-Ottawa Score (NOS) was used to evaluate the quality of the meta-included papers. NOS included three sec- tions (case selection, group comparison, and exposure de- termination) and eight elements. The quality rating scale went from 0 (worst) to 9 (highest) (best). Studies with a score higher than 5 were included. 2.2. Data extraction A pilot evaluation of the final full texts was performed to ensure inclusion of all data needed for final data synthesis to answer the study questions. Based on this evaluation, a checklist was provided for data extraction. This checklist in- cluded study ID, study design, province of study, duration of observation, the total number of cases (n), number of male and female cases, total mortality rate and mortality rate in each gender, and mean age of all participants, survivors, and non-survivors. A checklist of each study was filled by a sin- gle reviewer. Randomly, 5 studies were refilled by a second reviewer to ensure Inter-Rater reliability of checklists. 2.3. Data synthesis We quantitatively examined the mortality rates of aluminum phosphide poisoning, the gender ratio of mortality, and the age of individuals. Mean age was pooled using the random effect model through calculation of Standard Mean Differ- ence (SMD). The possibility of publication bias was checked using freeman-Tukey double arcsine transformation and Eg- ger’s test in case of the binomial outcome of mortality. In case of publication bias, the trim-and-fill approach was used to address the issue. All statistical analyzes were performed us- ing R statistical packages. 3. Results As shown in the PRISMA flowchart (figure 1), finally, 21 stud- ies with 3432 cases of ALP poisoning were included in this meta-analysis. There were about 1637 male and 1732 female poisoning cases (one study, Shadnia et al., 2007, did not re- port gender). Cases were evaluated from 2000 to 2021 (table 1). 3.1. Overall mortality rate The pooled mortality rate of ALP poisoning in Iran was 39.6% (95% CI: 31.5% to 47.9%); with 95% heterogeneity (p <0.01; figure 2). This open-access article distributed under the terms of the Creative Commons Attribution NonCommercial 3.0 License (CC BY-NC 3.0). Downloaded from: http://journals.sbmu.ac.ir/aaem 3 Archives of Academic Emergency Medicine. 2021; 9(1): e66 Table 1: Studies included in the meta-analysis Study* ID Year** N Gender (n) Age (year; mean ± SD) Male Female Total Survivor Died Majidi et al., 2021; (6); Urmia 2015- 2019 134 96 38 40 28.6±11.5 NA NA Navabi et al. 2018 (7); Kermanshah 2014- 2015 77 48 29 41 NA 28.7±10.2 31.3±10.7 Shadnia et al., 2007 (8);Tehran 2003 63 NA NA 8 NA NA NA Ataei et al., 2021 (9);Mashhad 2019- 2021 41 23 18 8 27.56±7.09 NA NA Mehrpour et al., 2008(10); Tehran 2006 45 24 21 32 27.3 ± 11.5 NA NA Rahbar et al., 2006 (11);Rasht 2000- 2003 116 63 53 68 29.47±14.79 NA NA Montazer et al., 2016 (12);Sari 2013-2014 52 14 38 16 23.4±9.2 NA NA Rahbar et al., 2013 (13);Rasht 2008-2009 104 66 38 93 33.8±14.69 NA NA Rahbar et al., 2011 (14);Rasht 2005-2006 102 68 34 77 29.75±14.34 NA NA Soltaninejad et al. 2012 (15);Tehran 2007- 2010 956 433 523 230 NA 24.5±8.19 27.32±11.31 Hassanian-Moghaddam et al. 2007 (16);Tehran 2005-2007 340 162 178 100 25.7± 9.2 NA NA Hosseinian et al., 2011 (17); Mazandaran 2007- 2008 102 46 56 19 28.5±12.4 28.66±12.75 24.92±9.51 Shokrzadeh et al., 2017(18);Gorgan 2008- 2015 53 37 16 16 NA NA NA Farzaneh et al., 2015 (19);Ardabil 2006-2012 386 72 314 95 NA NA NA Navabi et al., 2018 (7);Kermanshah 2014- 2015 118 75 43 41 NA 28.7±10.2 31.3±10.7 Shadnia et al., 2009 (20);Tehran 2000- 2007 471 246 225 146 NA 24.38 ± 8.81 30.87 ± 14.80 Mehrpour et al., 2009 (21);Tehran 2006- 2007 45 24 21 32 NA NA NA Erfantalab et al., 2017 (22);Tehran 2014 - 2015 39 27 12 15 31.0±11.3 30.5±11.7 (17–65) 31.8±11.1 (23–61) Mostafazadeh et al., 2011 (23) Tehran 2009 48 24 24 9 25.5±9.5 NA NA Tavakoli-Far et al., 2018 (24);Karaj 2006- 2011 67 36 31 30 NA NA NA Shayeste et al., 2017 (25);Gorgan 2009- 2016 73 53 20 25 27.47±16.75 NA NA * All study types were cross-sectional. ** Duration of observation. NA, not addressed. 3.2. Gender and mortality rate The male and female mortality rates were pooled from 12 studies listed in figure 3a and 3b. Proportion of morality in male patients was 62.3% (95% CI: 53.5% to 70.8%); with 80% heterogeneity (p < 0.01). The proportion of mortality in fe- male patients was 37.7% (95% CI: 29.2% to 46.5%); with 80% heterogeneity (p < 0.01). As shown in the funnel plot in figure 4. freeman-Tukey dou- ble arcsine transformation and Egger’s test revealed signifi- cant funnel plot asymmetry, indicating the possibility of pub- lication bias or small-study effects, P<0.01. It reveals that studies are shifted to the right. Linear regression test of fun- nel plot asymmetry also confirmed asymmetry (t = 2.23, df = 21, p = 0.0369). To address the publication bias, we utilized the trim-and-fill approach to look at the effect on the pooled estimate. Af- ter applying the trim-and-fill approach to account for miss- ing studies, the result was a symmetrical Egger funnel plot, which is shown in figure 5, where the linear regression test of funnel plot asymmetry was not significant (t = 0.17, df = 25, p = 0.8673). The mortality rate that should be considered for therapeutic purposes is 27.3% (95% CI: 18.9% to 36.5%) as shown in the new forest plot in figure 6, with the pooled proportion corrected for publication bias. 3.3. Mean age and mortality rate In a comparison of mean age of survivors versus non- survivors, a random effect model showed a significant dif- ference between survivors versus non-survivors, where sur- vivors had significantly lower age (SMD: -0.26, 95% CI: -0.37 to -0.15; p< 0.01; figure 7). Heterogeneity was not observed in the case of age comparison (I2=0%). 4. Discussion This study showed a mortality rate of about 40% along with a publication bias. When we used trim-and-fill correction, mortality rate decreased to about 27%, which seems to be far from the reality. There is no proper official data available to facilitate reaching a final decision on mortality rate and in our knowledge, and this is the first study in Iran giving a com- prehensive mortality rate for ALP poisoning. Also, there is a wide distance between the mortality rates of males and fe- males, and averaging to find the overall mortality rate of ALP poisoning does not seem reliable. Other studies have reported a 70–100% mortality rate, as re- viewed by Meena et al. (26). A 59.3% mortality rate was re- ported in Mathai and Bhanu study in 2010 (27). But Iranian studies have reported a wider range of mortality rates as Ab- dollahi and Mehrpour (28) reported the mortality rate to vary This open-access article distributed under the terms of the Creative Commons Attribution NonCommercial 3.0 License (CC BY-NC 3.0). Downloaded from: http://journals.sbmu.ac.ir/aaem F. Bagherian et al. 4 from 30 to 100%. But other factors, as well as the amount of consumed ALP, affect the results. Unfortunately, due to factors such as high toxicity and high lethality of this substance and ease of access to this toxin, based on official reports a relatively high rate of poisoning is seen in the country, especially in some provinces such as Tehran, Gilan, Mazandaran, Golestan, and Lorestan, (5). Our meta-analysis also showed that most published studies are performed in these provinces. Our study showed that the mortality rate of ALP poisoning in Iran was 39.6% with the proportion mortality being 62.3% in males and 37.7% in female patients. In the comparison of mean age of survivors versus non-survivors, there was a sig- nificant difference between survivors versus non-survivors, where survivors had a significantly lower age. Based on the reports by forensic medicine facility of Iran, most of the ALP-poisoning-related deaths were in the age group of 20-40 years, and most of them intended to commit suicide. Statistics from 2008 to 2011 show that death from rice pills were on the rise. There were 214 individual cases of mortality (105 women / 109 men) in 2008, 228 cases (104 women / 124 men) in 2009, 406 cases (202 women / 204 men) in 2010, and 463 cases (204 women / 259 men) in 2011 (5). In a comparison of studies performed outside Iran, accord- ing to El-Sarnagawy’s study, there was a strong link between mortality risk and young age, rural location, suicidal inges- tion, increased toxic dose, and prehospitalization duration. They reported 44.7% deaths with ALP in 5 years (29). A study by Sheta showed that 43.3 percent of cases died (30). Com- pared to our study, better survival in Iranian poisoning cases could be due to the higher experience of Iranian health care providers in the management of ALP poisoning, as most case reports of successful treatment of ALP are being published by Iranians (31-33). In a study by Alnasser et al., they evaluated ALP poisoning in Saudi Arabia over a nine-year period, the highest rate of death from AlP poisoning belonged to children, and it oc- curred most frequently during household fumigation. Delays in medical treatment and diagnosis may have had a role in the patients’ death (34). Poisoning due to the use of rice pills in Iran has led to the re- sponsible organizations and institutions in the country tak- ing measures to ban the import and restrict the sale of rice pills. Having comprehensive data on ALP poisoning mortal- ity rate in our country could help us in policymaking regard- ing public sale of ALP for industrial purposes. 5. Limitations A concern in this study was the possibility of publication bias. As a result, the findings of this study should be interpreted with caution, bearing the limitations in mind. Although our article search was limited to Iran, there was a low possibility of biased study retrieval due to the high number of studies; however, there might be a possibility of incomplete study re- trieval as we did not find studies performed in the south of the country and medical dissertations and official and unof- ficial reports were not included. Reporting bias might also have affected our results as datasets with high mortality rates might have not be reported. 6. Conclusion According to this report, the mortality rate of ALP poisoning in Iranian population is about 27%, with men having a higher fatality rate than women. Poisoning at a younger age is asso- ciated with better results. 7. Declarations 7.1. Acknowledgments We would like to thank the Clinical Research Development Unit of Peymanieh Educational and Research and Therapeu- tic Center of Jahrom University of Medical Sciences for pro- viding facilities for this work. 7.2. Funding This research did not receive any grant from funding agencies in the public, commercial, or non-profit sectors. 7.3. Conflict of interest statement The authors have declared that no competing interests exist. 7.4. Author contribution FB and NK conceptualized the study questions and per- formed revisions. FR and SA performed the searches. NH and NJM conducted the statistical analyses. Other authors provided the draft manuscript. 7.5. Ethical Considerations All ethical principles are considered in this article. References 1. Cienki J. Non-anticoagulant rodenticides. Clinical toxi- cology Philadelphia, PA: WB Saunders. [Book] 2001;858. 2. Lall S, Peshin S, Mitra S. Methemoglobinemia in alu- minium phosphide poisoning in rats. 2000 ;38(1):95-7. 3. 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Basic & clinical pharmacol- ogy & toxicology. 2016;118(3):243-6. 34. Alnasser S, Hussain SM, Kirdi TS, Ahmed A. Aluminum phosphide poisoning in Saudi Arabia over a nine-year period. Annals of Saudi medicine. 2018;38(4):277-83. This open-access article distributed under the terms of the Creative Commons Attribution NonCommercial 3.0 License (CC BY-NC 3.0). Downloaded from: http://journals.sbmu.ac.ir/aaem 7 Archives of Academic Emergency Medicine. 2021; 9(1): e66 Figure 1: PRISMA flow chart of study. This open-access article distributed under the terms of the Creative Commons Attribution NonCommercial 3.0 License (CC BY-NC 3.0). Downloaded from: http://journals.sbmu.ac.ir/aaem F. Bagherian et al. 8 Figure 2: Forest plot of mortality rate. Figure 3: Forest plot of mortality rate based on gender, (a) male, (b) female. This open-access article distributed under the terms of the Creative Commons Attribution NonCommercial 3.0 License (CC BY-NC 3.0). Downloaded from: http://journals.sbmu.ac.ir/aaem 9 Archives of Academic Emergency Medicine. 2021; 9(1): e66 Figure 4: Funnel plot of included studies. Figure 5: Trim-and-fill corrected Funnel plot of included studies. This open-access article distributed under the terms of the Creative Commons Attribution NonCommercial 3.0 License (CC BY-NC 3.0). Downloaded from: http://journals.sbmu.ac.ir/aaem F. Bagherian et al. 10 Figure 6: Trim-and-fill corrected Forest plot of mortality rate. This open-access article distributed under the terms of the Creative Commons Attribution NonCommercial 3.0 License (CC BY-NC 3.0). Downloaded from: http://journals.sbmu.ac.ir/aaem 11 Archives of Academic Emergency Medicine. 2021; 9(1): e66 Figure 7: Forest plot of mean age of survivors versus non-survivors. This open-access article distributed under the terms of the Creative Commons Attribution NonCommercial 3.0 License (CC BY-NC 3.0). Downloaded from: http://journals.sbmu.ac.ir/aaem Introduction Methods Results Discussion Limitations Conclusion Declarations References