An overview of bioaerosol load and health impacts associated with dust storms: A focus on the Middle East

Journal Pre-proof An overview of bioaerosol load and health impacts associated with dust storms: A focus on the Middle East Zahra Soleimani, Pari Teymouri, Ali Darvishi Boloorani, Alireza Mesdaghinia, Nick Middleton, Dale W. Griffin PII:

S1352-2310(19)30826-X

DOI:

https://doi.org/10.1016/j.atmosenv.2019.117187

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AEA 117187

To appear in:

Atmospheric Environment

Received Date: 11 July 2019 Revised Date:

24 November 2019

Accepted Date: 26 November 2019

Please cite this article as: Soleimani, Z., Teymouri, P., Boloorani, A.D., Mesdaghinia, A., Middleton, N., Griffin, D.W., An overview of bioaerosol load and health impacts associated with dust storms: A focus on the Middle East, Atmospheric Environment (2019), doi: https://doi.org/10.1016/j.atmosenv.2019.117187. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2019 Published by Elsevier Ltd.

An overview of bioaerosol load and health impacts associated with dust storms: A focus on the Middle East Zahra Soleimani1-2*, Pari Teymouri3-4, Ali Darvishi Boloorani5, Alireza Mesdaghinia2, Nick Middleton6 and Dale W Griffin*7 1

Department of Environmental Health Engineering, School of Public Health, Semnan University of Medical Sciences, Semnan, Iran

2

Department of Health Engineering, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran

3

Health and Environment Research Center, Tabriz University of Medical Sciences, Tabriz, Iran

4

Department of Environmental Health Engineering, Faculty of Health, Tabriz University of Medical Sciences, Tabriz, Iran

5

Department of Remote Sensing and GIS, Faculty of Geography, University of Tehran, Tehran, Iran

6

St Anne’s College, University of Oxford, Oxford OX2 6HS, UK

7

U.S. Geological Survey, 600 4th St. South, St. Petersburg, Florida 33701, USA

Corresponding Authors: Zahra Soleimani &Dale W Griffin

1

Abstract Dust storms are an important environmental problem worldwide. The main sources of dust storms include the Sahara, the Middle East, and central and northeastern Asia. Dust originating from these regions can be dispersed across oceans and in some cases globally. The storms occur throughout the year and vary in frequency and intensity. The biological agents (e.g., fungi, bacteria and viruses) and the mineral and chemical compositions of dust may have adverse effects on human health and quality of life. Desert dusts may cause respiratory diseases, cardiovascular diseases, cardiopulmonary diseases, mental health issues, injuries and death from transport accidents caused by poor visibility. This paper presents dust storm human health research conducted in the Middle East in both indoor and outdoor environments. Results illustrate that particle concentration and bioaerosol types in the atmosphere are affected by climate change and meteorological factors. Recent data trends indicate that annual dust aerosol concentrations have increased worldwide. According to studies conducted in the Middle East, the incidence of respiratory and cardiovascular mortality and hospital visits have increased dramatically following dust storm exposures but very few have demonstrated a regional causation. National and international collaborative research is needed to advance our understanding of the global implications of dust storms and what may be the most effective means of mitigation. Keyword: Dust storm, Middle East, Health, Bioaerosol

2

Introduction Sources and occurrence of dust in different locations and seasons in the Middle East Effect of climate change on dust storms The influence of environmental factors on the viability of microorganisms in the atmosphere Temperature Relative humidity Wind speed and direction Precipitation Season and time of day Other factors Health effects of bioaerosol (bacteria, fungi) exposure and detection Microbiology of Middle East dust storms Bacteria Fungi Viruses Conclusions

3

Introduction Sand and Dust Storms (SDS) are among the main environmental challenges in the world and although concentrated in drylands (Figure 1 and Figure 2), their impacts are felt beyond dryland boundaries due to long-range transport of desert dust (Griffin et al., 2007; Soleimani et al., 2015). The phenomena cause negative socio-economic, health, and environmental impacts in vulnerable regions including the Middle East1 (Middleton, 2017). SDS source mapping, associated bioaerosol load and their impacts are needed in the affected areas to deliver qualified and precise forecasts and other information for adaptation and mitigation efforts.

Figure 1. Global Dust Potential Map. Source: DTF (2013).

1

. In this paper the Middle East, south west Asia, and west Asia are the same and include the countries: Bahrain, Iran, Iraq, Jordan, Kuwait, Oman, Qatar, Saudi Arabia, Syria, Turkey, Yemen and the United Arab Emirates.

4

Figure 2. Atmospheric Aerosol Eddies, NASA Animated Map: 10km GEOS-5 Aerosol Optical Depth (AOD): Red/yellow colors are locations of dust aerosols. The largest areas with high aerosol values are located in the Northern Hemisphere, mainly in a broad band extending from North Africa to China (Prospero et al. 2002).

Along with environmental factors such as land surface vegetation cover, soil type, and water resources, atmospheric conditions cause formation of high-speed wind events that move large amounts of soil/bio dust from source areas to other regions. Based on the similarity in spatial distribution and regional atmospheric patterns, there are four clusters of dust-storm source regions across the Middle East that affect Iran (Figure 3) (Darvishi et al., 2012). The analysis of dominant atmospheric patterns in every cluster shows that there are two main dust emission patterns: the summer low pressure of Zagros (low pressure over the Iran plateau) and cyclonic and anti-cyclonic winter patterns. Within these main and subsidiary clusters are 5 types of terrain that typify SDS sources, i.e., agriculture fields, dried marsh/wetlands, seasonal riverbeds, degraded rangelands, and desert areas.

5

Figure 3. Four main trans-boundary SDS clusters affecting Iran All terrain types are sources of bioaerosol to the atmosphere with multi-faceted impacts that are classified as direct/indirect, tangible/intangible, and long-term/short-term effects. Iraq is the largest source of SDS, and Iraq, Kuwait, Iran, Qatar, Bahrain, UAE, Oman, Saudi-Arabia and other countries of the Persian Gulf are the most affected countries of the region. Iraq, Kuwait, and the southwestern parts of Iran and Iraq comprise the largest multi-country dust-storm source region in the Middle East and are the most disturbed by adverse regional dust storms. Accordingly, the city of Ahvaz, the capital of the Khuzestan province of Iran, was ranked as the world's most polluted city by the World Health Organization based on the regional average annual concentration of PM10 (particle matter 10 µm or less in diameter), in 2010 (Figure 4).

6

Figure 4. Cities with worst outdoor air pollution, WHO, 2010 7

Sources and occurrence of dust in different locations and seasons in the Middle East

One of the important parameters for understanding dust storms is to identify their source regions. These data allow the identification of their origins and transport mechanisms that permit strategies for prevention and remediation. Dust storms in southwest Asia are classified as one of two types: summer Shamal dust storms and non-summer frontal dust storms (including prefrontal, postfrontal and shear lines) (Abed et al., 2009; Cao et al., 2015). Cao et al., (2015) used the HYSPLIT model to identify SDS sources in west Asia from 2000-2013 and proposed 6 main SDS pathways in region that were based on climate systems, such as the Siberian and Polar anticyclones, monsoons from the Indian subcontinent, and geographical depressions in northeast Africa. Originating from the Mediterranean Sea and east Europe, the first and second paths are associated with summer Shamal winds. Paths from south of the Mediterranean Sea and/or north Africa (third and fourth paths) are associated with prefrontal dust storms in the summer or postfrontal dust storms in the winter. The fifth path also originates from North Africa and is associated with shear-line dust storms. The sixth path in west Asia originates from the Sistan plain along the Iran-Afghanistan border (Cao et al., 2015). Based on these paths, 6 sand and dust storm source-region clusters were also proposed by Cao et al., 2015). Cluster 1 lies in the first path of northeastern Syria and the Syria-Iraq border. Cluster 2 was the remainder source areas in Iraq and is the most severe Iraq SDS region. Cluster 3 is on the Iraq-Iran border and both Cluster 2 and 3 are affected by the first and second paths. These three clusters are located in the right side of the Tigris-Euphrates alluvial plain, which makes them the main SDS sources for Iran, Saudi Arabia, and other regional Arabian countries (e.g., Kuwait and Bahrain) (Cao et al., 2015) The source area in southern Syria, on the Jordan-Saudi Arabia border, and northwestern Saudi Arabia was considered as the fourth SDS source cluster and is under the influence of the fourth atmospheric pathway (south coast of the Mediterranean Sea or North Africa). The fifth source region gets hit by shear-line dust storms that originate in North Africa. The sixth and last source is located in Sistan and the Baluchistan Province of Iran, and dust from this region typically impacts air quality in Iran, Pakistan and Afghanistan (Cao et al., 2015)(Fig 5).

8

Figure 5. SDS main paths and source clusters in west Asia (Cao, et al., 2015). Rezazadeh et al., (2013) studied the synoptic features of land surface records of dust events over the Middle East from 1998-2003. They defined 4 regions based on the number of dust events and 4 conditions classified as dust in suspension, blowing dust, dust storm, and severe dust storm. The first region was Sudan, where the highest frequencies of dust in-suspension and severe dust storms happen due to Saharan dust intrusion. The second region included Saudi Arabia and Iraq, where relatively strong winds from the northeast and northwest dominate during dust events. The third region included Iran and Afghanistan, where the highest frequency of blowing dust and dust storms in the Middle East occur. Affected from the Thar Desert, the last region included Pakistan, where the highest mean concentration of airborne dust occurs. They found that dust events in the western part of the Middle East (i.e., from Sudan to Saudi Arabia and Iraq) happen more frequently in the winter. In the summer, they are more frequent in Pakistan and Afghanistan (Rezazadeh et al., 2013). Hamidi et al., (2017) used the WRF/Chem-D model to evaluate the 3-9 July 2009 severe duststorm events in the Middle East. They found that the Al-Nafud Desert and the western Euphrates alluvial plain, located in the west of Iraq, northwest of Jordan and eastern Syria, are the main dust source regions for that area (37°E, 25°N to 58°E, 38°N; contributing to more than 60% of dust emission over the Middle East). They also reported that although Iran was the source of 10% of dust storms, it was the deposition area for about 21% of emitted dust during the study 9

period. The average residence time of dust in the atmosphere of Iran was 7.8 days, which was longer than its duration over the studied area (6.2 days) (Hamidi et al., 2017). Taheri Shahraiyni et al., (2015) used the 28 Moderate resolution Imaging Spectroradiometer (MODIS) for the monitoring of dust storms in the Middle East to estimate their aerosol concentration during dusty days in 2008–2009. Their results showed that 60% of dust point sources in the Middle East are in Iraq and Syria (39.2 and 23%, respectively). Northern Saudi Arabia (14.5%), western Iran (13.8%), Jordan (5.7), and Turkey (3.8%) are the other dust point sources. The northwestern part of Iraq and the eastern part of Syria, the areas with low altitude and low vegetation cover, are the main source areas for dust storms in the Middle East (Taheri Shahraiyni et al., 2015). In a study by Al-Dabbas et al., (2011), satellite images of 27 dust storms blowing over Iraq, Saudi Arabia, and the Arabian Gulf in 2007-2008 were analyzed. Results showed that the majority of regional dust storms (80%) originate from Africa. These storms pass over the Mediterranean Sea to Syria, Jordan, or Turkey and then move over northern Iraq toward Saudi Arabia and the Arabian Gulf. The rest of the dust storms (less than 20%) came from southern Iraq (Al-Dabbaset al., 2011). By studying all the dust source regions in the Middle East in the period from 2001 to 2012, it was found that most of the sources are located in Iraq and Syria in comparison to the other countries of the region (Moridnejad et al., 2015). It has been reported that 144 out of 367 examined dust events in the Middle East have occurred in these regions. An area with severe desertification is located along the northwestern border of Iraq and Syria from Nineveh in Iraq to Al-Hasakah in Syria (Moridnejad et al., 2015). Moridnejad et al., (2015), found that the northern part of the Euphrates River between Tharthar Lake in Iraq and the Iraq-Syria border are also among the high- and low-intensity desertification areas that extend through the central and eastern parts of Iraq. After the Sahara Desert, Lower Mesopotamia is the second largest planetary dust source (Chudnovsky et al., 2017). Sand/dust storms in this region are affected by different factors such as hot weather in summers and low rainfall, which may cause drought conditions. Droughts become worse by ineffective irrigation (Chudnovsky et al., 2017) and mismanagement of water 10

in the region, such as constructed dams and water control strategies that have reduced regional water levels and caused severe drainage of soils in the Tigris and Euphrates basins (Moridnejad et al., 2015; Chudnovsky et al., 2017). Other factors are the high mountains and plateaus in neighboring countries that funnel air masses into the region (Sissakian et al., 2013; Chudnovsky et al., 2017). Blowing of strong, sustained, periodic and seasonal winds result in Shamal and Sharki sandstorms that may last for hours to days throughout the region (Chudnovsky et al., 2017). Abandoned farms are another reason for dust storms in this region (Sissakian et al., 2013).

Being the major part of Mesopotamia, Iraq has the highest number of dust storms (Chudnovsky et al., 2017). Depending on the geographical location, up to 122 sand and dust storms may happen in Iraq annually. Dust-storm-related activity in the Tigris and Euphrates basin starts in late spring (May), reaches its highest intensity in summer (July), and generally subsides by fall (September–November)(Al-Dabbas et al., 2012; Chudnovsky et al., 2017).

Deserts in Iraq, Syria, Kuwait, the Arabian Peninsula, and in North Africa are the common dust sources of dust storms in Iran (Shahsavani et al., 2012; Ashrafi et al., 2014; Marzouni et al., 2016; Maleki et al., 2016; Naimabadi et al., 2016). Hoor Al-Hoveyzeh lagoon in southwestern Iran (Najafi et al., 2014), the Kavir desert in central Iran (Khazaei et al., 2016) and the dried Jazmurian Lake in southeastern Iran are other sources for dust storms in Iran (Rashki et al., 2013). Results of a study by Cao et al., (2015) showed that the Al-Howizeh/Al-Azim marshes (still keeps expanding) and the Sistan Basin are the main SDS source areas in Iran (Cao et al., 2015). Indeed, the periodically dry shallow lakes of the Sistan Basin have long been recognized as one of the most active dust sources in the Middle East (Middleton, 1986a, 1986b; Rashki et al., 2015). Dust storms in Iran occur mainly in the late spring (May) (Shahsavani et al., 2012) and in the summer (June-July) although some dust events in Iran occur in the winter (Shahsavani et al., 2012; Ashrafi et al., 2014; Najafi et al., 2014; Hosseini et al., 2015; Maleki et al., 2016; Goudarzi et al., 2014; Marzouni et al., 2016)(See Table I). Located in the eastern Mediterranean area, Jordan is primarily impacted by Khamaseen dust storms several times each year during a 50-day period that typically extends from late March to early May (Abed et al., 2009; Hamasha et al., 2015). Kuwait suffers dust events (sand/dust storms, rising dust, and suspended dusts) approximately 13% of calendar days each year. Kuwait is subject to severe dust storms during 11

the spring and summer seasons (Saeed et al., 2014). Daytime dust events in Kuwait occur 25% of the time from April to August (Al-Awadhi and AlShuaibi, 2013). Dust storms in Kuwait occur 5% of annual calendar days, with 70% of them occurring during the daytime from March to August (Saeed et al., 2014; Al-Awadhi and AlShuaibi, 2013; Al-Dousari and Al-Awadhi, 2013).

12

Study

Study

location

Period

Iraq

1997–

Particle Matter (PM) type and

Dust Source

Season

-

Highest

reference

concentration (µg/m3) -

2010

mean

aerosol

(Chudnovs

optical depths (AOD) in

ky et al.,

summer

2017)

(May-July):

Maximum in July Lowest mean AOD in fall (September–November) Iraq

December

3 dust storm in winter (1 in

(Al-

(Baghdad,

2008

December 2008 and 2 in

Dabbas et

Ramadi, Kut,

March

February, 2009)

al., 2012)

Basra, Najaf,

2009

4 dust storms in spring

-

western desert of Iraq

to

Karbala, Hilla,

(March 2009) and

Tikrit cities) Iraq

spring and

-

summer

northwestern and western

spring and summer

region of Iraq

(Lateef et al., 2015)

2012 Iraq

December

Mean

2011 until May 2012

-

A dust event in winter:

(Ahmady-

TSP (total suspended

February 25 to March 3,

Birgani et

particles):325.8±284.54

2012. In Abadan

al., 2015)

PM10:181.8±53.19

Higher TSP and PM2.5 in

PM2.5: 171.25±91.16

spring compared to winter

Max: TSP=440 on May 1926, 2012 PM10=259 on March 512, 2012 PM2.5:303 on May 1926, 2012 Winter mean: TSP:231.33 PM10:175.33 PM2.5:110.50 Spring Mean: TSP:467.50 PM10:191.5 PM2.5:232.00

13

Table I: Summary of the studies on dust events in the Middle East Table I: Continued

Study location

Iran

(Abadan

city)

Particle Matter (PM)

Study

type

Period

and

Dust Source

Season

reference

3

concentration (µg/m )

2011 and

PM10

Iraq and Arabian

Winter mean of PM10 in

(Marzouni

2012

Annual mean

Peninsula

the studied period (2011

et al., 2016)

2011:148

and 2012) was higher than

2012:116

summer mean

Max: 2011:731in winter 2012:586 in summer Summer mean 2011:126 2012:126 Winter mean 2011:171 2012:126 Iran

(Ahvaz

city)

Iran

Overall Mean

Iraq, Kuwait, and Saudi

the temporal trends in the

(Shahsavan

Septemb

PM10: 319.60±407.07

Arabia

mean

and

i

er 2010

PM2.5:69.50±83.2

values

of

PM1:37.02±34.9

PM2.5,

Max:

concentrations over the

April-

May 18,

(Kermanshah city)

June 8 ,

and

study period reached peaks in May-June

PM1:495.3

Maximum PM was in June

PM10

western Syrian Desert

et

al.,

2012)

PM1

PM10:5337.6

May 18 : 496 th

PM10,

PM2.5:910.9

th

2010

maximum the

Maximum PM10 in was in

(Ashrafi et

June

al., 2014)

th

June 8 :625

2010 Iran city)

(Ahvaz

2009-

PM10

Sahara Desert and deserts

The temporal trends in the

(Maleki

2014

Overall mean:249.5

in Iraq, Saudi Arabia, and

mean values of the PM10

al., 2016)

Overall Max:420.5 in

Kuwait

concentrations over the

July

study

Overall Min:154.6 in

peaks in June-July

January

Maximum PM10 was in July

14

period

reached

et

Table I: Continued Study

Study

Particle Matter (PM) type

location

Period

and concentration (µg/m3)

Iran (Ahvaz

December

city)

2012 - until June 2013

Dust Source

Season

PM10

Iraq, Saudi Arabia,

Although

mean

(Naimabadi

Total mean:483

and

concentration of PM10 in the

et al., 2016)

Winter:

Sahara Desert

Kuwait,

the

reference the

dusty days of winter were

Normal days:

higher

than

in

spring,

Mean ± SD:117±38

maximum concentration of

Min:54

PM10 was observed in dusty

Max:195

days of spring

Dusty days: Mean 510 ±664 Min:204 Max:2862 Spring Normal days: Mean ± SD:129 ±40 Min:58 Max:195 Dusty days Mean:457 ±586 Min:204 Max:4443 Iran

April

(Sanandaj

September

city)

2013

to

PM10

Iraq

June among the other months

(Hosseini et

Overall mean:160.63

has the highest mean PM10

al., 2015)

Min:31.14 in May

concentration

Max:837.12 in June

214.68, µgm3) and spring

mean on

had a higher mean PM10

Normal days:96.88

concentration than summer

(273.49

±

Dust days:472.28 Iran (Qom

July 2011 -

PM10:

Central desert of Iran

Overall mean concentrations

(Khazaei et

city)

June 2012

Overall Mean:207.3±136.7

known as Kavir

of PM in the studied period

al., 2016)

Max 1160.67 in September

showed the following order:

PM2.5:

summer>fall>spring>winter

Mean: 61.8 ± 38.1 Max:242.92 in September PM1 Mean:21.3± 12.5 Max:90.82 in September

15

Table I: Continued Study

Particle Matter (PM) type

Period

and concentration (µg/m3)

Iran

1) 4 April

Mean TSP

1) Kermanshah,

2011

Ahvaz,

2) 13 April 2) 3,900

Qasreshirin

2011

Arabian Peninsula,

2) Kermanshah,

3) 3 June 4)

Ahvaz,

2011

Mahshahr

4)

3) Kermanshah,

April 2012

Desert,

Ahvaz,

5) 24 May

Hoor Al-Hoveyzeh

Mahshahr,

2012

lagoon in Khuzestan

Study location

1) 1,953

3) 4,500 315

Dust Source

Season

reference

Iraqi desert, desert

Among the spring dust

(Najafi et

lands in the north

events, June 2011 had the

al., 2014)

and

highest TSP concentration

northeast

of

east and southeast

5) 1,003

of

19-20

Syria,

also

occasionally Sahara

Qasreshirin

province,

4) Kermanshah,

southwest of Iran

in

the

Qasreshirin 5) Kermanshah, Ahvaz, Qasreshirin Iran

(Ahvaz

city)

November

Mean

The highest mean and

(Goudarzi

2011

PM10:598.92

maximum values of the

et

PM2.5:114.8

PM10, PM2.5, and PM1

2014)

PM1:34.5

were observed in March

to

May 2012

-

al.,

2011 Overall

mean

concentrations

of

showed

following

the

PM

order:winter>spring>fall Jordan (Amman

North African

Maximum AOD values

(Hamasha

and AzZarqa in

Sahara

were in spring (March -

et

the middle, and

Egypt)

May); AOD values were

2015)

Ma’an

2003-2012

-

(usually

in

up in spring, down in

southern Jordan)

summer, up in autumn,

al.,

and then down in winter Jordan (western

March

mountainous

May, 2006

part)

to

Size Fraction

North African

Spring (late March - early

(Abed

•Most PMs: 5–20 µm

Sahara (Libya)

May)

al., 2009)

•All samples were strongly skewed toward 15 µm. •PM≤5 µm: up to 16% •PM≤10µm : 8 to 49%.

16

et

Table I: Continued

Study location

Kuwait

Particle Matter (PM)

Study

type

Period

and

Dust Source

Season

Spring

referenc e

concentration (µg/m3)

26

PM10:

- Around Kuwait and the

March

2641

southern parts of Iraq

2003

(Saeed et al., 2014)

- the Rub’al Khali in the central-southeastern

parts

of the Arabian Peninsula Kuwait

February

PM10

Eastern

side

of

the

Overall mean concentrations

(Alolaya

(Kuwait City)

2004 and

Annual mean: 130±106

Mediterranean region

October

Fall:115

of PM in the studied period

n et al.,

showed the following order:

2013)

2005

Winter:83

spring>summer>fall>winter

Spring:162 Summer:138 PM2.5 Annual mean:53±58 Fall:49 Winter:29 Spring:58 Summer:57 Kuwait

January

PM10 mean

Countries in the Arabian

Warm

(Kuwait City)

1996–

Annual:212 (Ranged 0-

Peninsula

summer)>cool seasons (fall-

and

Decembe

5038)

winter)

Taiar,

r 2000

Cool

season

(Oct-

season

(spring-

(Thalib Al-

2012)

Apr):137 (Ranged: 04999) Warm season (May to Sep.):314 (Ranged 05038) Lebanon El-Fil

(Sin located

in

the

southeastern suburb

17

th

and

18

th

of

-

Iraq and Syria

Spring

(Borgie et

May,

al.,

2016)

2011 of

Beirut) Lebanon

Novemb

PM:10-2.5

(Beirut)

er

between 10 and 53)

and

(Ranged

Decembe

PM2.5 (Ranged between

r 2012

21 and 39)

African and Arabian deserts

Fall

(Jaafar et al., 2014)

17

Table I: Continued Particle Matter (PM) Study location

Study Period

type

and

concentration

Dust Source

Season

reference

1) Saharan desert

1) Spring

(Dada

2) Arabian deserts

2) Fall

al., 2013)

(µg/m3) Lebanon

1) March 14th,

(Beirut)

2013

-

et

2) November 22nd, 2012 Lebanon

February

(Beirut)

2004

27th

Arabian (southeast)

Overall mean concentrations

(Saliba

2005:

and

of PM in the studied period

al., 2007)

PM (10-2.5):102.5

(southwest) in the fall

showed the following order:

PM2.5:67.4

and spring mild seasons

fall>winter>summer>spring

-

Spring

•1) until

January 2005

February

Saharan

Deserts

et

th

•2) 7 May 2004: PM (10-2.5):64.9 PM2.5:25.4 •3)29 September 2004: PM (10-2.5):93.4 PM2.5:59.9 •4) 15th October 2004: PM (10-2.5):111.7 PM2.5:42.9 Lebanon

February

(Beirut)

May of 2003

-

Maximum

PM10

in

March:238

(Shaka and Saliba, 2004)

th

Saudi

10-11

Arabia

March, 2009

-

Qasim area, Adibdibah

Early spring

and As-Summan Plateau

(Alharbi et al., 2013)

for 10th March dust storm Western Iran for 11th March dust storm Saudi Arabia

March 2012

Mean ± SD on dust-

March 3rd and 13th: South

storm days

of Jaddagh th

PM10:909±641

March

many areas on the coast

PM2.5:247±165

of the Red Sea

PM1:40±25

March 22nd: North and east of Jaddagh

18

(Alghamdi et al., 2015)

th

PM2.5-10:663±477

17

Spring

and18 :

Table I: Continued Particle Matter (PM) Study location

Study Period

type

and

Dust Source

Season

reference

Sahara Desert

High levels of PM10 were in

(Kabatas et

Winter: 111.5 ±29.6

winter, due to local and

al., 2014)

Spring: 80.3±32.5

regional pollution sources

Summer: 62.5±15.5

April 14 had the highest PM

Fall: 72.5±20.9

concentration due to Saharan

concentration (µg/m3)

Turkey

2008

PM10 mean:

(81 cities)

Max

daily

average:

170 in April 14 Turkey

1996

(Erdemli)

1999

and

dust

th

-

North

Africa

and

(Koçak

occasionally from the

et

al., 2004)

Middle East Turkey

October

(Erdemli)

2007-April

-

Middle

East

and

(Koçak

Saharan desert dusts

et

al., 2012)

2008 Egypt

Max PM2.5

Khamasin, Winter and

(Embaba,

Dust days:250

like-winter type are the

and

Giza)

Hazy dust days:130

kinds of dust storms

Khoder,

attacking Egypt

2017)

Egypt

2013-2014

1989-1995

-

-

(Hassan

the surrounding

Spring had the highest number

(Zakey

(Cairo and

desert and local sources

of dust storms, but the values

al., 2004)

Aswan)

of wind-blown dust

of

Cairo

city

is

also

aerosol

optical

characteristics in fall were

surrounded by Mokatm

higher than spring until the

Hill,

end of the fall season.

which

provides

Cairo with fine sand during strong spring

and

autumn

winds

#+# = mean+standard deviation (SD) for those studies where SD was provided.

19

et

Effect of climate change on dust emissions

Climate can contribute significantly to the quantity of surface soil particulates that are aerosolized and can move vast distances in Earth’s atmosphere each year. Analyses of ice core sections that dated ~14,000 to 16,000 years ago (Ice Age in the Pleistocene Epoch) demonstrated that the quantity of dust moving through Earth’s atmosphere was much greater than what was observed ~10,000 years earlier (Thompson, 2001). This is due as much more of Earth’s water is entrapped as ice resulting in a reduction in sea level, a corresponding increase in land cover and arid lands. Periods of drought and large-scale standing atmospheric pressure oscillations such as the North Atlantic Oscillation (NAO) are known to contribute significantly to the annual quantity of dust emissions from the Sahara and Sahel (Middleton, 1985; Griffin, 2009). The NAO has been in a more positive state since the mid-1960’s and this period has corresponded with the current prolonged North African drought. Climate cycle events such as El Nino are known to amplify annual region dust emissions on a global scale (Griffin, 2009, 2010). Local meteorological conditions (surface wind speed, precipitation) and local surface characteristics (e.g., vegetation cover, soil moisture, sediment availability) are two important drivers causing dust emissions and may vary at different timescales and trends (seasonal, interannual and decadal).

Anthropogenic activities can contribute to wind erosion both directly, especially

through agricultural and deforestation activity, and indirectly via social (lack of environmental stewardship support, etc.), economic (profit-oriented, etc.) and political philosophy (problem awareness and recognition, etc.), over various timescales. These drivers of change may occur synergistically and at multiple scales over time (Middleton, 2019). Future climate change projections indicate that drylands are expected to expand worldwide (Feng and Fu, 2013; Huang et al., 2016), with increases in the risk of periods of drought (Dai, 2013) and an increase in dust emissions (Pu et al., 2017). The influence of environmental factors on the viability of microorganisms in the atmosphere

Different environmental factors have been reported to play influential roles in composition and survival of airborne microorganisms. Among them, precipitation, temperature, relative humidity, and wind speed and direction are factors affecting bioaerosol composition and microbial viability and function (Jones and Harrison, 2004; Burrows et al., 2009; Smets et al., 2016). 20

Temperature Temperature may directly affect the metabolism and survival of bioaerosols and indirectly affect through prolonged suspension periods that may be due to induced boundary-layer turbulence (Burrows et al., 2009). At near freezing temperatures, most microorganisms have limited metabolic activity. Significant differences in metabolic activity and survival are known at temperatures above freezing and are due to genetic differences among diverse microbial community members (Mocali et al., 2017; Zhong et al., 2016). In adverse atmospheric conditions, Gram-positive bacteria are more resistant than Gram-negative bacteria. That is why in samples of warm air of Ahvaz city in Iran, Gram-positive bacteria were more dominant (Soleimani et al., 2014; Goudarzi et al., 2014; Soleimani et al., 2016). AlDabbas et al., (2011) also found that gram-positive Bacillus species are more common than other genera of bacteria (Al-Dabbas et al., 2011). In their study on the bacteria concentrations during dust-event days in Ahvaz, Soleimani et al., (2014) reported linear correlations between the total concentrations of bacteria and Bacillus spp. with temperature. Correlations between total fungi concentration and temperature have been reported by different researchers (Çeter and Pinar, 2009; Asan et al., 2010). Viable spore forming bacteria and fungi are commonly recovered in regional and long-range aerosol transport studies due to the ability of spores to shield cellular material from UV, temperature related stress and humidity extremes (Kellogg and Griffin, 2006, Griffin, 2007; Smith et al., 2011; Smith et al., 2018). Brągoszewska and Pastuszka 2018 reported a significant positive correlation between temperature and bacterial bioaerosol concentrations in autumn and winter (cold seasons): but, a negative correlation in summer and spring (warm seasons). During cold seasons, fluidity of cell membrane and then microbial activity are decreased by the low temperatures. Increased ambient temperature causes bacterial growth and release, which is the reason for the positive association. On the other hand, in warm seasons, the higher temperature is related to strong ultraviolet radiation, which is not suitable for the bacterial reproduction and inhibits their growth and leads to the denaturation and inactivation of proteins (Di Giorgio et al., 1996; Liu et al., 2015; Mouli et 21

al., 2005; Chi and Li 2007; Fang et al., 2007; Wang et al., 2010; Wu et al., 2012; Zhong et al., 2016). Relative humidity This environmental factor can affect other factors impacting the viability of bioaerosols. High relative humidity (RH) may act as a protective cover for bacteria against UV light or carbon monoxide (Tang, 2009). Moderate linear correlations between the concentration of Streptomyces spp. and Bacillus cereus with relative humidity were noted in air samples from Ahvaz city (Soleimani et al., 2014). Asan et al., (2010) also reported a strong positive correlation between total fungal species and relative humidity in a rural area in Turkey. But, monthly mean relative humidity (< %50) had a strong negative correlation with total fungal concentrations in air samples collected from Ankara (Çeter and Pinar, 2009). Zhong et al., (2016) noted no significant difference between microbial activity and relative humidity, due to no significant change during the study period. Bacterial growth is enhanced by higher water availability due to metabolism needs. Aggregation of bacterial cells can also occur in high RH conditions and this can increase the survival of cells within the aggregates that are shielded by more external cells (Kallawicha et al., 2015). The integrity of cell walls and viral capsids can be altered by RH, which can promote growth and aerosolization (Jones and Harrison 2004; Soleimani, et al 2015; Brągoszewska and Pastuszka 2018). At low RH, microbial activities decrease due to the scarcity of water (Zhong et al., 2016).

Precipitation Some bioaerosols may increase after rainfall (Jones and Harrison 2004; Burrows et al., 2009). For example, Alternaria spore concentrations showed a positive correlation with rainfall (Herrero et al., 1996). Sabariego et al., (2000) reported significant negative correlation coefficients between rainfall and airborne Alternaria spore concentrations. Çeter and Pınar (2009) noted that rainfall showed strong negative correlations with fungal spore concentrations in samples from Ankara.

22

Wind speed and direction Wind at a speed above 8.0 m/s transfers the dust particles from surface soil to the atmosphere (Kim and Chung, 2010; Gonzalez-Martin et al., 2013). Desert top soils consist of diverse prokaryote communities (Papova et al., 2002; Griffin, 2007; Gonzalez-Martin et al., 2013) with one gram typically containing between 104 to 107 bacterial cells (Whitman et al., 1998; Griffin, 2007; Gonzalez-Martin et al., 2013). Brągoszewska and Pastuszka (2018) and Li et al., (2017) could not find significant association between microbial concentrations and wind speed. Zheng et al., (2016) did not find significant correlations between wind direction and microbial activity in their studied period. Wind direction did not affect fungal concentration significantly during a study period in Qatar (Al-Subai, 2002). To find precise relationships between wind speed and bioaerosol concentrations, large data sets are needed. Bioaerosol concentrations need to be analyzed over wind speed ranges of less than 1 km h−1 to more than 20 km h−1 (Brągoszewska and Pastuszka, 2018; Li et al., 2017). Higher wind velocity may result in longer range transport and higher microbial concentrations (AlSubai, 2002; Çeter and Pinar, 2009; Asan et al., 2010), but it may also cause a decrease in microbial activity via wind-driven dehydration of non-spore-forming microorganisms (Griffin, 2007). Season and time of day Seasonality can also play an important role in bioaerosol concentrations in the atmosphere as dust storms all over the world display marked seasonality. In a study by Zhong et al., (2016) in China,

microbial

activity

in

bioaerosols

showed

a

seasonal

variation

of

summer>autumn>winter>spring. Significant differences were found between bioaerosol activities in the summer and spring, summer and winter, fall and spring, and fall and winter.

Al-Dabbas et al., (2011) reported the highest values of isolates of bacteria and fungi occurred in the late spring months and early summer season due to increased dust events during these periods. Candida albicans had relatively high concentrations in May and July, which is believed to be due to high temperatures, high evaporation, and low relative percent humidity. Such 23

conditions result in increased rates of fungi growth in soil and regional atmospheric suspension due to generation and activity of dust storms (Al-Dabbas et al., 2011). According to the findings by Najafi et al., (2015), the abundances of bacteria and fungi were the most during April to June, due to optimum temperature and the relative humidity. They also indicated that the dust storms in western Iran mostly occur in the spring. Thus, microbial concentrations were the highest in this season (Najafi et al., 2014). Other regional studies have also shown that the highest concentration of air-borne microorganism occurs in the spring (Asan et al., 2010; Morris et al., 2011). Bacterial viability in the summer might be less than in other seasons due to stressors such as ozone, humidity, and solar radiation, which lead to an ecological shift due to the survival of more adapted species (spores forming bacteria)(Smets et al., 2016).

Fungal species such as Cladosporium and Alternaria may be present in the atmosphere in high concentrations even under conditions of low humidity and high wind speed, especially during warm afternoon periods (Troutt and Levetin 2002; Asan et al., 2010). In a study on airborne fungi in Qatar, the highest total colony counts of fungi were at 12 PM (high temperature) and the lowest at the hours 12 AM and 6 AM (lower temperature) (Al-Subai, 2002). Other factors

Bacterial concentrations may also be affected by human activities such as automotive traffic, agriculture and population density and by vegetation and plants type and coverage (Fang et al., 2007; Heo et al., 2017; Akpeimeh et al., 2019). Several studies have shown that bacterial concentrations at locations in populated areas with high traffic flows are high; and in greener areas with less human activity are comparably low (Mouli et al., 2005; Fang et al., 2007; Goudarzi et al., 2014). In contrast, some studies have shown that fungi concentrations at rural and farming areas are high (Tarigan et al., 2017; Lee et al., 2006; Thilsing et al., 2015). Grampositive bacteria in comparison to gram negatives show greater resistance and survival ability to stress sources such as desiccation, strong sunlight and aerosolized chemical pollutants (Fang et al., 2007). Low levels of vegetation can result in elevated temperatures, and dryness has been identified as the reason for higher atmospheric concentrations Gram positive bacteria in Ahvaz, Iran (Soleimani et al., 2015; Goudarzi et al., 2014).

24

Health effects of bioaerosol (bacteria, fungi) exposure

Particle matter (PM) size distribution affects type and concentration of bioaerosols in the atmosphere. Bertolini (2013). Gandolfi et al., (2012) concluded that different bacterial communities could be present in different PM fractions. Paraskevi et al., (2008) reported that most of their bacteria were detected at respirable size fractions (< 3.3µm in size) and many were phylogenetic neighbors to human pathogens that cause diseases such as pneumonia, meningitis, and bacteremia, or have been associated with the induction of pathologic reactions such as endocarditis

(i.e., Streptococcus

gordonii, Haemophilus

pneumoniae, Streptococcus

parainfluenzae, Acinetobacter

mitis, Streptococcus lwoffi, Acinetobacter

johnsonii, Propionibacterium acnes).

Desert dusts have adverse effects on human health. The biological agents (e.g., fungi, bacteria, and viruses) and the mineral and chemical compositions of dust, such as silicate, carbonates, oxides, sulfates, mercury, cadmium, arsenic, and salts, may have adverse effects on human health and quality of life. There are many studies of desert dust storms and health risks (Griffin, 2007; Sandstrom and Forsberg, 2008; Goudie, 2014; Sprigg, 2016; Soleimani et al.,2019 a). As illustrated in Table 2, many studies have shown that desert dusts are associated with mortality and morbidity due to respiratory diseases (e.g., asthma, pneumonia, rhinitis, tracheitis, silicosis, and coccidiomycosis), cardiovascular diseases (arrhythmia, ischemic heart disease, stroke, and cerebrovascular disease), cardiopulmonary diseases (chronic obstructive pulmonary disease), and injuries and death from transport accidents caused by poor visibility. In addition, it may cause mental health affects due to stress (Perez, 2012; Ma et al., 2016; Middleton, 2008; Sprigg, 2016). In the Middle East (Iran, Iraq, Kuwait, and Saudi Arabia), hospital admissions can be high during dust events. Particles which can penetrate into lungs (PM10) and deep into the lung subepithelial environment (PM2.5) can cause human-health risks (Griffin, 2007). Mortality due to cardiovascular and respiratory disease, respiratory hospitalization, upper respiratory tract infection, pneumonia, and hypertension are health issues that have significant association with dust storms (Meng and Lu, 2007; Soleimani et al., 2019 b) (Table 2).

25

Table 2: Summary of studies on human health and desert dust storms Study location

Study

Lag time

Effect on health Significant associations were found between outdoor air pollution concentrations and daily emergency room (ER) visits for respiratory diseases in the spring dust season; and mostly between PM (particulate matter)10, SO2 and NO2 and ER visits on dust days for elderly females, elderly males, and adult males, respectively. Cardiovascular and respiratory mortality due to PM2.5–1 during Saharan dust days were about the double compared to non-dust days, but these differences were not statistically significant.

Period China

2007-2011

1-7 days

Spain

2004-2009

lag 1 day for cardiovascular and cerebrovascular mortalities and lag 2 days for respiratory mortality

Taiwan

1998-2007

same days, lag7 and non-dust days

Spain

2003-2005

lag 0-4 days

U.S.

1993-2005

lags 0-5 days

Japan and Korea

2005-2011

lag 0-5-days

Japan

2005-2010

lag 0-6-days

Cyprus

1995-2004

Iran

2010

lag 0 = same day or lag 1, 2 = previous two days Same day

The relative rate of children's respiratory clinic visits significantly reduced to 0.74-0.99 in most districts during Asian dust storm (ADS) periods, whereas it rose to 1.01 1.11 in more than half of districts during post-ADS periods. An increase of 10 mg m-3 of PM10–2.5 caused a raised total mortality of 2.8% during Saharan dust days. Significant associations with non-accidental mortality were estimated for 2 states (California at lag 2 and 0-5 days) and Arizona (at lag 3), for cardiovascular mortality in the United States (lag 2) and Arizona (lag 3), and for other nonaccidental mortality in California (lag days 1-3 and 0-5). An increase of 10 mg/m3 of PM10 was significantly associated with an elevated relative risk (RR) of all-cause mortality at the same day (lag 0) and previous day (lag 1) (RR:1.003 and 1.001, respectively) and cerebrovascular disease (RR:1.006 at lag 1) in Seoul and western Japan (cities of Nagasaki and Matsue) but, no significant associations were observed in Tokyo, which is situated farther from the origin of Asian dust. Asian dust adverse association with mortality was independent of suspended particulate matter (SPM). It did not change the effects of SPM on mortality and had stronger effects on northern areas, close to its source. A 10 µ/m3 increase in the mean concentration of the current to the previous 2 day’s worth of Asian dust caused an excess risk of 0.6%, 0.8%, 2.1%, and 0.5% for heart disease, ischemic heart disease, arrhythmia, and pneumonia mortality, respectively.

reference Ma et al., 2016

Perez,et al., 2012

Yu, et al., 2013

Tobías 2011

et

al.,

Crooks 2016

et

al.,

Kashima et al., 2016

Kashima et al., 2012

In dust-storm days, 4.8% and 10.4% higher all-cause and cardiovascular admissions were reported, respectively.

Middleton et al., 2008

1% increase in dust-caused air pollution results in about 0.5 %, 1% and 0.3% increased respiratory, cardiac, and the heart disease mortality, respectively. But, statistically significant

Delangizan al., 2013

26

et

Iran

2009 2010

-

Iran

2015-2016

Iran

2017

Same day

Spain

2003-2004

0-4 days after dust

China

2001-2005

lags of days 1-6 after dust

Taiwan

1997-2007

0-7 lag days after dust

Korea

2001-2009

0-5, lag effect of dust storms up to 7 days

Kuwait

2009 2011

Same day

Spain

2004-009

4 -11 days

China

1994-2003

a lag of between 1 and 6 days following a dust event (lag 1–6).

-

Same day

relationship between dust phenomenon and respiratory diseases was not observed. Significant association between PM10 level and number of cardiovascular services during dust events was found. But, such association was not observed between PM10 level and emergency service. The excess cases for cardiovascular/respiratory morbidity were observed as 20/51 on normal, 72/185 on dusty, and 20/53 on MED event days. PM10 concentrations above 10 µg/m3 were estimated to be responsible for 4.7% and 4.2% of hospital admissions for respiratory and cardiovascular diseases, respectively. The level of the risk of illnesses for citizens exposed to dust with the rate of eolian sediment exposures in the was statistically significant. Human ecosystems (1) Dehno-Piran, (2) Bazzi-Allari, (3) Muhammad-Shah-Karam, and (4) AbbasRostam regions in the Sistan area have the highest risk levels for respiratory illnesses and eye afflictions caused by eolian sediment dispersion exposures. During Saharan dust days, an increase of 10 g/m3 in daily PM10-2.5 concentration caused an increased daily mortality of 8.4%. But no increased risk of daily mortality was observed for PM2.5. Sand-dust weather showed an association with the increased hospitalizations for respiratory diseases and with lagging effects. the health effect of sand-dust weather, on males and people aged ≥65 years was more severe compared with their effects on females, and on those aged <65 years. Children had increased clinic visits for respiratory diseases in the week after exposure to Asian dust storms (ADS). Significant positive associations between ADS and mortality at lag 0 (cardiovascular: 2.91%; males: 2.74%; and <65 years: 2.52%), at lag 2 (males 2.4%; and <65 years: 2.49%), at lag 3 (total non-accidental: 1.57%, males: 2.24%; and <65 years: 2.43%;) and at lag 5 (cardiovascular: 3.7%; and males: 2.04%) in the model which additionally adjusted for NO2. The study has concluded that pollen of Malvaceae, Compositae and Chenopodiaceae was the most common triggers of allergy in Kuwait. Additionally, a positive correlation between the number of allergy patients and deposited dust was observed during March 2010 and 2011. Particulate matter (PM) on days with Saharan dust intrusions was associated with daily mortality, indicating Saharan dust as a possible risk factor for daily mortality. Dust events were significantly associated with total respiratory hospitalization for males and females (with a lag of 3 days and relative risks (RR) of 1.14 and 1.18, respectively); upper respiratory tract infection (URTI) in males (with a lag of 3 days and RR 1.28), and pneumonia in males, (with a lag of 6 days and an RR of 1.17. Dust events also showed a significant association with hypertension in males (with a lag of 3 days and RR 1.30). In the seasonal analysis model, respiratory hospitalizations in spring and cardiovascular hospitalizations in winter had stronger association with dust events.

27

Ebrahimi et al., 2014

Khaniabadi al., 2017

et

Sahebzadeh al., 2019

et

Perez 2008

et

al.,

Tao et al., 2012

Yu et al., 2012

Lee et al., 2013

Al-Dousari al., 2018

et

Díaza 2017

et

al.,

Meng 2007

et

al.,

Greece

2001-2006

Same day

Greece

2001-2006

1 day

Italy

2002-2006

0-4 days after dust

Kuwait

1996-2000

1-5 days after the storm events

Kuwait

1996-2000

1-5 days after the storm events

Kuwait

2012

Same day

China

2004-2005

1-5 days

japan

2011-2013

2-6 days

Taiwan

1997-2007

0-5 days after dust

Nigeria

2010-2011

Same day

Saudi Arabia

2011-2012

exposure to sandstorm for the period of 24±2.68 minutes

An increase of 1.95% in respiratory emergency-room visits was associated with a 10-µg/m3 increase in PM10 concentration. But such association was not observed with desert dust episodes. Desert dust days were significantly associated with higher emergency-room visits for asthma (38%), chronic obstructive pulmonary disease (57%), and respiratory infections (60%) An increase of 10 µg/m3 in PM10 was associated with a 0.71% increase in all deaths. Total and cause-specific mortalities were mostly reported for those ≥75 years of age. Females were those who showed higher effects in the form of total mortality. Desert-dust days and its interactions with PM10 levels significantly affected all cases except for respiratory and cardiovascular mortalities among those of <75 years of age. Increased respiratory mortality was observed for people of ≤75 years of age on Saharan dust days (SDD), by 22.0% on the SDD in the whole year model and by 3.9% in the hot season model. Odds Ratio for natural and cardiovascular mortality were 1.042 and 1.043, respectively, which shows a lower effect of SDD on them. During the five-year study period, a significant association was observed between days with dust-storm events and an increased risk of same-day asthma and respiratory admission, especially for children (adjusted relative risk of 1.07 and 1.06, respectively). Originated from crustal materials, local dust, did not have significant effect short-term respiratory (RR=0.96), cardiovascular (RR = 0.98) or all-cause mortality (RR = 0.99). PM10 concentrations were significantly correlated with bronchial asthma at the 0.05 level (Pearson r = 0.292). Significant correlations at the 0.01 level were shown between bronchial asthma and both acute lower respiratory tract infection (r = 0.737) and acute upper respiratory tract infection (r = 0.839). Respiratory and cardiovascular mortality rates were both equal to 0.62 per 10,000 persons, each corresponding to 8.7% proportionate mortality rate. PM2.5 concentration during dust events was associated with the increased outpatient visits of respiratory (including total respiratory diseases and its two subgroups: upper respiratorytract infection, and pneumonia) and cardiovascular (including total cardiovascular diseases and its subgroups: hypertension and ischemic heart diseases) diseases. During high desert-dust days, pregnant women showed an increased risk of allergic symptoms. Simultaneous dispersion of Japanese cedar pollen and positive IgE in those women was observed which resulted in an increased odds ration OR. Compared with weeks before ADS events, the clinic visits during weeks after ADS events showed an increase of 2.54% and 5.03% times for pre-school and school children, respectively. Respiratory infections including asthma, bronchitis and pneumonia were responsible for more than 20% of infant mortality and morbidity during Saharan dust events. Cough (47.77%), runny nose (51.06%), wheeze (33.46%), acute asthmatic attack (20.88%), eye irritation/redness (48.74%), headache (34.62%), body ache (38.5%), sleep and psychological disturbances (30.36% and 37.52%,

28

Trianti 2017

et

al.,

Samoli 2011

et

al.,

Zauli Sajani et al., 2017

Thalib and AlTaiar, 2012

Al-Taiar and Thalib, 2014

Al-Hemoud al., 2018

Zhang 2013

et

et

al.,

Kanatani et al., 2016

Chien 2012

et

al.,

Uduma and Jimoh, 2013

Meo et al., 2013

respectively) were among the complaints reported by subjects who were exposed to the sandstorm in Riyadh.

Besides mineral compounds, desert dust consists of organic compounds including microorganisms, which may have a negative impact on human health in regional and downwind areas via pathogenesis, exposure of sensitive people to cellular compounds (e.g., pollen, fungal allergens, lipopolysaccharide, etc.) and development of sensitivities such as asthma due to longterm exposure (Griffin, 2007). The Middle East is among the areas with the highest incidence of asthma on Earth. (Griffin, 2007). Al Eskan disease is pneumonia acquired from dust-storm exposure and was reported among military personnel deployed in the Persian Gulf war (Griffin, 2007). Bacillus genera among bacteria and Aspergillus spp. among fungi have been reported to be the dominant microorganisms during periods of dust storms in Iraq (Al-Dabbas et al., 2012), Saudi Arabian (Kwaasi, 2003) and Iran (Najafi et al., 2014). Well-known examples of dust storm-associated human disease due to microbial infections are the annual West African meningococcal meningitis outbreaks (Garcia-Pando et al. 2014; AlDabbas et al., 2011; Smets et al., 2016). Neisseria meningitidis (the causative agent of meningitides in West Africa) was isolated in dust samples collected in Kuwait (Griffin, 2007; Leski et al., 2011). Microbiology of Middle East dust storms Table 3 lists the genus and species, where identified, from samples collected in the Middle East during dust events and includes method of collection and identification, sample site location and dust-source region. Bacteria Mycobacterium spp. that was detected in breathable dust from arid areas of Iran and Kuwait

(Leski et al., 2011) and Sanandaj city in Iran (Nourmoradi et al., 2015) may be involved in respiratory diseases (Leski et al., 2011). Brucella spp. are zoonotic pathogens causing brucellosis in livestock. Brucella suis, one of the

detected Brucella spp. in arid areas of Iran and Kuwait, is a potential biowarfare agent. Although 29

direct or indirect exposure to infected animals is the common pathway for human infections with Brucella species (e.g., B. melitensis and B. abortus), direct infection via inhalation of pathogen-

contaminated aerosols is also possible (Leski et al., 2011). Coxiella burnetii, another potential biowarfare agent, was detected in arid areas of Iran and

Kuwait, which indicates a high prevalence of this organism in the examined samples (Leski et al., 2011). Streptomyces spp. was found in air samples of Ahvaz, Iran (Goudarzi et al., 2014; Soleimani et al., 2016) and Erdemli, Turkey (Griffin et al., 2007). Bacillus spp. as potential human pathogens (Griffin, 2007), were detected in dust samples in the

west of Iran (Najafi et al., 2014), arid regions of Iran and Kuwait (Leski et al., 2011), Ahvaz, Iran (Goudarzi et al., 2014; Soleimani et al., 2016), Sanandaj, Iran (Nourmoradi et al., 2015), and Erdemli, Turkey (Griffin et al., 2007). Kocuria spp. (the agent identified in advanced noma lesions (Griffin, 2007), were detected in

dust samples of Ahvaz, Iran (Goudarzi et al., 2014) and Erdemli, Turkey (Griffin et al., 2007). Kocuria rosea (bacteremia agent) was also detected in breathable dust samples of Erdemli,

Turkey (Griffin et al., 2007). Bacillus circulans and B. licheniformis are known opportunistic human pathogens associated with dust storms (Al-Dabbas et al., 2011) . Pseudomonas aeruginosa, which might cause a fatal infection in burn patients (Griffin, 2007) was found in

samples from Sanandaj, Iran (Nourmoradi et al., 2015) and different cities in western Iran (Najafi et al., 2014). Micrococcus spp. (opportunistic pathogen, particularly in hosts with immunocompromised systems) were detected in breathable dust samples in western Iran, (Najafi et al., 2014) and Ahvaz, Iran (Soleimani et al., 2016). Staphylococcus aureus causes a wide range of infections and is a potential human pathogen. It was found in airborne dust in Middle East (Awad, 2007; Al-Dabbas et al., 2011) and in western Iran (Najafi et al., 2014). Species of Klebsiella (commonly found on soil and dust) and Enterobacter (found in soil and airborne dust) are known pathogens and species of these genera have been detected in airborne dust in the Middle East (Awad, 2007; Al-Dabbas et al., 2012; Najafi et al., 2014). Escherichia coli, a common to human gut flora has been isolated from airborne dust (Al-Dabbas

et al., 2012; Najafi et al., 2014). Clostridium perfringens, Bacillus cereus, Corynebacterium sp., Paenibacillus sp., Microbacterium sp., Arthrobacter sp., Bacillus subtilis and Streptomyces

30

ambifaciens were other bacteria that were detected in breathable dust of the Middle East. (Leski

et al., 2011; Goudarzi et al., 2014; Nourmoradi et al., 2015; Griffin et al., 2007). Some airborne bacteria may produce compounds that are dangerous to human health. Lipopolysaccarides (LPS) are endotoxins and part of cell walls of Gram-negative bacteria, which can cause illness through inhalation. Exposures to lipopolysaccharides can elicit strong immune responses (Smets et al., 2016). Fever and reduced airflow in the lungs are short-term symptoms, and development of asthma and bronchitis, or even irreversible damage in the respiratory tract can result from long-term exposure to LPS (Griffin, 2007). For LPS to effect human health, it is not necessary for bacteria cell to be viable (Smets et al., 2016). Desert dust passing over coastal environments may adsorb aerosolized Gram-negative bacteria from marine aerosols and transport them considerable distances inland. Such events may happen when African dust passes over coastal areas in the Middle East and be a contributing reason for the high incidence of asthma in this region. (Al Frayh et al., 2001; Griffin, 2007). Fungi

Since PM2.5 and PM10 frequently contain different allergens and pathogens, including fungi, exposure to fungal spores (typically 2-10 µm in size) may result in allergenic reactions such as asthma (exposures can be lethal due to mycotoxins) (Black et al., 2000; Griffin et al., 2007), hypersensitivity of pneumonitis (Dehghan et al., 2014), allergic and invasive aspergillosis (as the most common invasive mold infection worldwide) (Soleimani et al., 2013). Fungal sinusitis and invasive fungal infections are other health problems that might affect the immune compromised (Ascioglu et al., 2002; Dehghan et al., 2008; Dehghan et al., 2014). Small sized fungal spores (usually less than 10 µm) (e.g. Aspergillus and Penicillium) may reach the alveoli, whereas those species with larger sized spores tend to be deposited in the upper sections of the respiratory system (Kurup et al., 2000). A. flavus spores ( 3 to 6 µm ) tend to infect paranasal sinuses and has been reported to be the etiologic agent of rhinosinusitis, in both healthy and immunocompromised people in Iran (Dehghan et al., 2008; Dehghan et al., 2014). Cladosporium, Alternaria, Penicillium and Aspergillus are dominant in arid climates as their

spores are pigmented and thus more resistant to ultraviolet damage (Abu-Dieyeh et al., 2010). Fungi such as Candida spp., Cryptococcus neoformans, Aspergillus fumigatus, and Histoplasma

31

capsulatum produce β-glucan. Being the most abundant fungal cell wall polysaccharide in

human fungal pathogens, β-glucan is also one of the most important pathogen-associated molecular patterns (PAMP) that is detected upon fungal infection and trigger host immune responses.

Immune effects of β-glucan is attributed to its ability to bind to the receptors

dispersed on the cell surface of phagocytic and cytotoxic innate immune cells, including monocytes, macrophages, neutrophils, and natural killer cells. Cell types and receptors involved characterize observed immune responses (Camilli et al., 2018).

According to the World Allergy Organization Alternaria and Cladosporium (in Kingdom of Saudi Arabia (KSA), Kuwait, Qatar, Jordan, Turkey, Egypt and Iran), Aspergillus (in KSA, Kuwait, Qatar, UAE, Jordan, Turkey, Egypt and Iran), Penicillium (in KSA, Kuwait, Qatar, Jordan, Turkey, Egypt, Iran and Morocco), Ulocladium (in KSA, Kuwait, Qatar, Jordan, Egypt, Iran and Morocco) and various other fungi (in KSA, Kuwait, Bahrain, Jordan, Egypt, Turkey and Iran) are recognized allergens in the Middle East (WAO). Aspergillus spp. were isolated from dust storms in Iraq during March 2007 to June 2008 (Al-Dabbas et al., 2011) and two spring seasons of 2011 and 2012 in western Iran (Najafi et al., 2014). Over 20 species are recognized as opportunistic human pathogens and a number of different allergen-related disease types in immunocompromised individuals (Griffin, 2007). For example, Aspergillus niger may be responsible for human health issues such as extrinsic alveolitis, allergic bronchopulmonary aspergillosis, keratitis, endophthalmitis, primary cutaneous aspergillosis and necrosing otitis (Abu-Dieyeh et al., 2010). Alternaria was one of the prevalent fungal genera that were isolated from dust samples collected

in Erdemli, Turkey in 2002. Alternaria spores are known allergens, and childhood exposure in semi-arid environments may cause asthma development (Griffin et al., 2007). Alternaria alternaria has been reported to be an potent agent of respiratory stress (Ozkara et al., 2007). Cladosporium sp. were among the fungi found in air samples from Sanandaj on dusty days

(Nourmoradi et al., 2015). Cladosporium sp. are often involved in allergenic fungal cases (Green et al., 2006). They may also interact with airborne pollen and enhance allergic response (Darvishi Boloorani et al., 2012), C. cladosporioides, and other species of Cladosporium may cause phaeohyphomycosis (Kantarcioglu et al., 2002). C.herbarum, is often the major cause of inhalant allergy and allergic asthma in humans (Abu-Dieyeh et al., 2010). Penicillium sp. can 32

cause broncho pulmonary penicilliosis, hypersensitivity, allergic alveolitis and other allergenrelated disease. Mucor sp. are opportunistic pathogens and this genera was the most frequently isolated in Middle East Springtime Dust Storm (MESDS) in western of Iran (Najafi et al., 2014). Microsporum sp. (can cause dermatophytosis) and Chrysosporium sp. (an opportunistic pathogen

that can infect brain, nasal and skin tissue)(Griffin, 2007) were also detected in air samples from Sanandaj during dusty days (Nourmoradi et al., 2015).

Viruses

Viruses are known to be the most numerous entities on earth at an estimated population of ~1031 (Breitbart and Rohwer, 2005). Viruses are known to exist in any environment where cellular life exists regardless of inhospitable and harsh the environmental conditions may be (Griffin, 2013). In regard to desert soils viruses have been shown to range from ~103 to 107 per gram of soil and that those number may vary considerable across a given desert transect (Gonzalez-Martin et al., 2013). A one-log increase in virus-like particle counts over background (no visible atmospheric dust) counts was observed when Saharan/Sahel dust was present in the atmosphere over the U.S. Virgin Islands (Griffin et al., 2001). Scientist in Taiwan demonstrated a higher likelihood of detecting influenza virus genomes in the atmosphere when desert dust from China’s deserts was impacting Taiwan’s atmosphere (Chen et al., 2010). Outbreaks of Foot-and-Mouth Disease have been noted in livestock following Chinese dust storm events impacting Korea and Japan (Ozawa et al, 2001; Joo et al, 2002; Sakamoto and Yoshida, 2002) although scientists were not able to detect it in collected dust samples (Ozawa et al, 2001; Joo et al, 2002). Recently, GonzalezMartin et al. (2018), noted a higher detection frequency of human enteric viruses in the atmosphere occurred when Saharan/Sahel dust storms were impacting the air quality of Tenerife, Spain. Atmospheric eubacteria isolates collected during dust storm events where shown to produce virus-like particles following exposure to the induction agent mitomycin C (TeigellPerez et al., 2019). The data from this study indicates that bacteria and other microorganisms like fungi and protozoa may serve as viral carriers and thus deliver intact virulence genes (antibiotic resistance, toxin, etc.) to distal ecosystems (Teigell-Perz et al., 2019). In respect to the number of studies of dust storm microbiology that have been conducted and published in scientific literature, and there are not many, very few published papers, as cited above, have been 33

conducted on dust storm virology. These few studies demonstrate potential global scale implications and the need for a clearer understanding of the risks that dust storm viruses may play in ecosystem and human health.

Table 3. Genera of bacteria and fungi found in Middle East dust storm samples (identified to at least the genus level)

Bacterial and fungal genera and concentrations

Method of identification (bacterial/fungal)

Location (reference)

Dust source region

Chrysosporium sp. Cladosporium sp. Mycosporium sp. Mycobacteriaum sp. Pseudomonas aeruginosa Bacillus sp. the mean concentration of total bacteria 1995 (CFU/m3) and mean total fungi 2268 (CFU/m3).

Andersen single-stage impactor (28.3 L/min) for 2.5 min. Microscope/microscope biochemical tests

Sanandaj, Iran (Nourmoradi et al., 2015)

Iraq and Saudi Arabia

Staphylococcus sp, Streptomyces sp. Bacillus sp, Micrococcussp.Corynebacterium sp, Stomatococcus sp, Dermabacter sp, Rhodococcus sp. Brevibacterium sp. Deinococcus sp. Arthrobacter sp. Bacillus cereus. Cellulomonas sp. Nocardia sp. Arthobacter sp.

Andersen single-stage impactor (28.3 L/min) for 2.0 min.

Ahvaz, Iran (Soleimani, Parhizgari et al., 2015)

Iraq and Saudi Arabia

Andersen single-stage impactor (28.3 L/min) for 2.0 min. Microscope/microscope biochemical tests

Ahvaz, Iran (Soleimani et al., 2013)

Iraq and Saudi Arabia

Andersen single-stage impactor (28.3 L/min) for 2 -15min

Ilam, Iran (Mazloomi et al., 2016)

Iraq and Saudi Arabia

Using a deployable particulate sampler (DPS) system (SKC Inc., Eighty-Four, PA) equipped with a PM10 size-selective inlet allowing collection of particles of 10 m or

Kuwait and Iraq (Leski et al., 2011)

Arid areas of Iraq and Kuwait

Gram-negative:

Microscope/microscope Biochemical tests

Achromobacter sp.Pseudomonas sp. Enterobacter sp. Serratia sp. Klebsiella pneumonia, Acinetobacter sp. the mean concentration of total bacteria indoor 804.3 (CFU/m3 ) Aspergillus sp. Alternaria sp. Cladosporium sp. Penicillium sp Rhizopus sp. total fungi indoor 676.5 (CFU/m3). Cladosporium, Penicillium, Aspergillus and Alternaria the mean concentration of total fungi 567 (CFU/m3 ) Mycobacterium sp. Brucella sp. Coxiella burnetii Clostridium perfringens Bacillus sp. Coxiella burnetii,

34

smaller in aerodynamic diameter. The particles were collected for 24 h from the sampled air at a rate of 10 liters per min on 47-mm, 2-m-pore-size polytetrafluoroethylene (PTFE) filters reinforced with a PMP support ring (SKC Inc.) Multiplexed PCR and a high-density resequencing microarray (RPM-TEI version 1.0) Deinococcus sp. Pseudomonas sp. Gordonia sp. Pandora cu sp. Microbacterium sp. Nocardia sp. Staphylococcus sp. Amycolatopsis sp. Corynebacterium sp. Kocuria sp. Streptomyces sp. Bacillus mean concentration of total bacteria during the study Period was 620.6 CFU/m3.

Using a microbial air sampler (Quick Take-3, SKC, USA), operating with a flow rate of 14.3 L/min

Ahvaz, (Goudarzi 2014)

et

Iran al.,

Iraq and Saudi Arabia

The species or genera of the cultured dishes were identified based upon their micro- and macro morphological characteristics, based on standard taxonomic keys

Limitations of available data

There are few published research projects focused on the measurement and identification of bioaerosols in the Middle East. Bioaerosols have historically been studied using different methods with many studies using non-standardized culture-based approaches and similar variation in approach is seen in the few molecular based studies. Many studies have reported impacts of environmental factors on bioaerosols but many of these studies are seasonal in nature and thus the observations may miss annual trends. Those studies that reported health effects of dust storm exposure have been focused on the association of hospital admissions and mortality. Other data sources that may provide additional insight into the extent of the influence such as clinics have not been surveyed. Many of these limitations of data sets are driven by funding constraints and there is a recognized need for standardized ‘Big Data’ studies. Conclusion

Recently, climate change driven decreases in precipitation and water crises have resulted in increased dust levels in some parts of the Middle East. During the last two decades the main sources of dust in the Middle East are from degraded lands, dried agriculture and wetlands of Iraq and Syria, the Sahara Desert and the deserts of Saudi Arabia. Particle concentration and bioaerosol types in the atmosphere are affected by climate change and meteorological factors.

35

For example, elevated temperature is favorable for some aerosolized microorganisms such as Aspergillus and Bacillus, and for others such as Cladosporidium and Micrococcus higher

humidity is favorable. Dust events occur in different seasons. According to most studies, in some regions in the Middle East (like southwest of Iran, central and southeast of Iraq, Kuwait and northwest of Saudi Arabia) the highest occurrence of dust events was is in the summer, although in some other regions (like northwest of Persian Gulf regions in Iran, Iraq, and Kuwait) winter and spring were the peak seasons. Studies have also shown the concentrations of bioaerosols in dust storms have significantly increased. Some of bioaerosols (bacteria, fungi and viruses) have adverse human health effects. According to studies conducted in this area, the incidence of respiratory and cardiovascular mortality and hospital visits have increased dramatically following dust storm exposures. It is worth noting that climate change and global warming have led to increases in desertification and the frequency of dust storms. Water resource management and the prevention or mitigation of desertification may reduce human, environmental and economic risks associated with dust storms. Regional, national and international collaborative research is needed to advance our understanding of the global implications of dust storms and what may be the most effective means of mitigation. Acknowledgement/Disclaimer This research was supported by both Semnan University of Medical Science in Iran,and the U.S. Geological Survey's Environmental Health Toxic Substances Hydrology and Contaminate Biology Programs. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government. The views and opinions expressed herein reflect those of the U.S. Geological Survey but may or may not state or reflect those of other agencies of the United States government and shall not be used for advertising or product endorsement purposes.

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References Abed, AM., Kuisi, MA., & Khair, HA.2009. Characterization of the Khamaseen (spring) dust in

Jordan. Atmospheric Environment. 43, 2868-2876. Abu-Dieyeh, M. H., Barham,R., Abu-Elteen,K., Al-Rashidi,R., Shaheen,I. 2010. Seasonal variation of fungal spore populations in the atmosphere of Zarqa area, Jordan. Aerobiologia. 26, (4), 263–276. Ahmady-Birgani, H., Mirnejad, H., Feiznia, S., Mcqueen,K G. , 2015. Mineralogy and geochemistry of atmospheric particulates in western Iran. Atmospheric Environment. 119, 262-272. Akpeimeh, G.F., Fletcher, L .A., Evans, B.E. 2019. Exposure to bioaerosols at open dumpsites: A case study of bioaerosols exposure from activities at Olusosun open dumpsite, Lagos Nigeria. Waste Management. 89, 37-47 Al Frayh, A.R., Shakoor, Z., Gad E.l Rab, M.O., Hasnain, S.M. 2001. Increased prevalence of asthma in Saudi Arabia. Ann. Allergy Asthma Immuno. 86(3), 292-296. Al-Awadhi, J. M. and AlShuaibi, A. A. 2013. Dust fallout in Kuwait city: Deposition and characterization. Science of the Total Environment. 461-462, 139-148. Al-Dabbas, M., Abass M.A and Al-Khafaji, R. M, 2012. Dust storms loads analyses-Iraq. Arabian Journal of Geosciences. 5, 121-131. Al-Dabbas, M., Al-Abbas, M.A. and Ahmed, M. 2011. The mineralogical and micro-organisms effects of regional dust storms over Middle East region. International. Journal of Water Resources and Arid Environments. 1(2), 129-141. Al-Dousari, A., Al-Awadhi J. and Modi, A. 2012. Dust fallout characteristics within major global dust storm trajectories. Arabian Journal of Geosciences. 6(10), 3877–3884. Al-Dousari, A. M., Ibrahim, M. I., Ahmed, N. M., Al-Awadhi, S. 2018. Pollen in Aeolian dust with relation to allergy and asthma in Kuwait. Aerobiologia. 34, 325–336. Alghamdi, M., Almazroui, M., Shamy, M., Redal,M.A., Alkhalaf,A.K., Hussein M.A., Khoder ,M.I. 2015. Characterization and elemental composition of atmospheric aerosol loads during springtime dust storm in Western Saudi Arabia. Aerosol and Air Quality Research.15, 440-453. Alharbi, B., Maghrabi, A.H. And Tapper, N. 2013. The March 2009 dust event in Saudi Arabia precursor and supportive environment. American Meteorological Society .51794(4), 515528. 37

Al-Hemoud, A., Al-Dousari, A., Al-Shatti, A., Al-Khayat, A., Behbehani, W and Malak, M., 2018. Health impact assessment associated with exposure to PM10 and dust storms in Kuwait. Atmosphere. (9)6, 1-13. Alolayan, M.A., Brown, K.W., Evans J.S., Bouhamra ,W.S., Koutrakis ,P., 2013. Source apportionment of fine particles in Kuwait City. Science of the Total Environment. 448, 1425. Al-Subai, A.A.T. 2002. Air-borne fungi at Doha, Qatar. Aerobiologia. 18, 175-183. Al-Taiar, A. and Thalib, L. 2014. Short-term effect of dust storms on the risk of mortality due to respiratory,

cardiovascular

and

all-causes in

Kuwait.

International

Journal of

Biometeorology. 58, 69–77. Asan, A., Sarıca Okten, S. and Sen, B. 2010. Airborne and soil borne microfungi in the vicinity hamitabat thermic power plant in Kirklareli City (Turkey), their seasonal distributions and relations with climatological factors. Environmental Monitoring and Assessment.164, 221231. Ascioglu,S., Rex, J.H., DePauw, B., Bennett, J.E., Bille, J., Crokaert, F., Denning, D.W., Donnelly, J.P., Edwards, JE., Erjavec, Z., Fiere, D., Lortholary, O., Maertens, J., Meis, JF., Patterson, T.F., Ritter, J., Selleslag, D., Shah, P.M., Stevens, D.A. and Walsh, T.J. Invasive Fungal Infections Cooperative Group of the European Organization for Research and Treatment of Cancer; Mycoses Study Group of the National Institute of Allergy and Infectious Diseases. 2002. Defining opportunistic invasive fungal infections in immunocompromised patients with cancer and hematopoietic stem cell transplants: An international consensus. Clinical Infectious Diseases.34, 7-14. Ashrafi, K., Shafiepour-Motlagh, M., Aslemand, A. and Ghader, S. 2014. Dust storm simulation over Iran using HYSPLIT. Journal of Environmental Health Science and Engineering. 12 (9), 1-9. Awad, A. 2007. Airborne dust, bacteria, actinomycetes and fungi at a flourmill. Aerobiologia. 23, 59-69. Bertolini, V., Gandolfi, I., Ambrosini,R., Bestetti, G., Innocente, E., Rampazzo, G. and Franzetti, A. 2013. Temporal variability and effect of environmental variables on airborne bacterial communities in an urban area of Northern Italy. Applied Microbiology and Biotechnology. 97(14), 6561-70. Black, P. N., Udy, A.A. and Brodie, S.M. 2000. Sensitivity to fungal allergens is a risk factor for life-threatening asthma. Allergy. 55, 501-4. Borgie, M., Ledoux, F., Dagher, Z., Verdin, A., Cazier, F., Courcot, L., Shirali, P., GreigeGerges, H. and Courcot, D. 2016. Chemical characteristics of PM2.5–0.3 and PM0.3 and consequence of a dust storm episode at an urban site in Lebanon. Atmospheric research, 180, 274-286.

38

Bragoszewska, E. and Pastuszka, J.S. 2018. Influence of meteorological factors on the level and characteristics of culturable bacteria in the air in Gliwice, Upper Silesia (Poland). Aerobiologia. 34, 241–255. Breitbart, M. and Rohwer, F. 2005. Here a virus, there a virus, everywhere the same virus? Trends in Microbiology. 13, 278-284. Burrows, S.M., Elbert, W., Lawrence, M.G. and Pöschl, U. 2009. Bacteria in the global atmosphere – Part 1: Review and synthesis of literature data for different ecosystems. Atmospheric Chemistry and Physics. 9, 9263-9280. Cao, H., Amiraslani, F., Liu, J. and Zhou, N. 2015. Identification of dust storm source areas in West Asia using multiple environmental datasets. Science of the Total Environment. 502, 224-235. Cao, H., Liu, J., Wang, G., Guang, Y. and Lei, L. 2015. Identification of sand and dust storm source areas in Iran. Journal of Arid Land. 7(5), 567-578. Camilli, G., Tabouret, G. and Quintin, J. 2018. The complexity of fungal β-glucan in health and disease: effects on the Mononuclear Phagocyte System. Frontiers in Immunology. 9, 19 Çeter, T. and Pinar, N.M. 2009. Atmospheric concentration of fungus spores in Ankara and the effect of meteorological factors in 2003 period. Mikrobiyoloji Bülteni.43, 627-638. Chien, L. C., Yang, C. H., and Yu, H. L. 2012. Estimated effects of Asian dust storms on spatiotemporal distributions of clinic visits for respiratory diseases in Taipei children (Taiwan). Environmental Health Perspectives. 120(8), 1215–1220. Chudnovsky, A.A., Koutrakis, P., Kostinski, A., Proctor, S.P. and Garshick, E. 2017. Spatial and temporal variability in desert dust and anthropogenic pollution in Iraq, 1997-2010. Journal of the Air & Waste Management Association 67(1), 17–26. Crooks, J.L., Cascio, W.E., Percy, M.S., Reyes, J., Neas, L.M. and Hilborn, E.D. 2016. The Association between dust storms and Daily non-accidental mortality in the United States, 1993-2005. Environmental Health Perspectives. 124 (11), 1735-174. Dada, L., Mrad, R., Siffert, S., Saliba, N.A. 2013. Atmospheric markers of African and Arabian dust in an urban eastern Mediterranean environment, Beirut, Lebanon. Journal of Aerosol Science.66, 187-192. Dai, A. 2013. Increasing drought under global warming in observations and models. Nature Climate Change 3, 52 Darvishi Boloorani, A., Nabavi S.O., Azizi, R. and Bahrami, H. A. 2012. Characterization of dust storm sources in Western Iran using a synthetic approach. Advances in Meteorology. Climatology and Atmospheric Physics. 415-420. Dehghan, P., Zaini, F., Rezaei, S., Jebali, A., Kordbacheh, P. and Mahmoudi, M. 2008. Detection of aflr gene and toxigenicity of Aspergillus flavus group isolated from patients with fungal sinusitis. Iran Journal Public Health. 37(3), 134-141. Dehghan, P., Kharazi, M., Rafiei, H., Akbari, M. and Paria, G.R. 2014. Enumeration and identification of dust fungal elements from the weather inversion phenomenon in Isfahan, Iran. Advanced biomedical research. 3, 120. 39

Delangizan, S. and Motlagh Z.J. 2013. Dust phenomenon effects on cardiovascular and respiratory hospitalizations and mortality—A case study in Kermanshah, during MarchSeptember 2010–2011. Iranian Journal of Health and Environment. 6, 65–76. Díaz, J., Linares, C., Carmona R., Russo, A., Ortiz, C., Salvador, P. and Trigo, R.M. 2017. Saharan dust intrusions in Spain: Health impacts and associated synoptic conditions. Environmental Research. 156, 455–467. DTF (Integrated Desert Terrain Forecasting for Military Operations) 2013. Earth and Ecosystem Sciences. https:// www.researchgate.net/figure/276048930_fig1_Figure–10–Global–Dust– Potential–Map–After–DTF–2013 Ebrahimi, S.J., Ebrahimzadeh, L., Eslami, A. and Bidarpoor, F. 2014. Effects of dust storm events on emergency admissions for cardiovascular and respiratory diseases in Sanandaj, Iran. Journal of Environmental Health Science & Engineering. 12, 110. Fang, Z., Ouyang, Z., Zheng, H., Ang, X., Hu, L. 2007. Culturable airborne bacteria in outdoor environments in Beijing, China. Microbial Ecology. 54, 487-496. Feng, S. and Fu, Q. 2013. Expansion of global drylands under a warming climate. Atmospheric Chemistry and Physics. 13, 10081–10094. García-Pando, C.P., Thomson, M.C., Stanton, M.C., Diggle, P.J., Hopson, T., Pandya, R., Miller, R.L. and Hugonnet, S. 2014. Meningitis and climate: from science to practice. Earth Perspectives, 1(1),14. Gonzalez-Martin, C., Teigell-Perez, N., Lyles, M., Valladares, B., Griffin, D.W. 2013. epifluorescent direct counts of bacteria and viruses from topsoil of various desert dust storm regions. Research in Microbiology.164, 17-21. Gonzalez- Martin, C., Coronado-Alvarez, N.M., Teigell-Perez, N., Diaz-Solano, R., Exposito, F.J., Diaz, J.P., Griffin, D.W. and Valladares, B. 2018. Analysis of the impact of African dust storms on the presence of enteric viruses in the atmosphere in Tenerife, Spain. Aerosol and Air Quality Research. 18(7), 1863-1873. Goudarzi, G., Shirmardi, M., Khodarahmi, F., Hashemi-Shahraki, A., Alavi, N., Ankali, K., Babaei, A., Soleimani, Z. and Marzouni, M. 2014. Particulate matter and bacteria characteristics of the Middle East Dust (MED) storms over Ahvaz, Iran. Aerobiologia. 30(4), 345-356. Goudie, A.S. 2014. Desert dust and human health disorders. Environment International. 63,101113 Green, B., Tovey, E., Sercombe, J.K., Blachere, F.M., Beezhold, D.H. and Schmechel, D. 2006. Airborne fungal fragments and allergenicity. Medical Mycology. 44(1), 245-255. Griffin, D.W., Garrison, V.H., Herman, J.R. and Shinn, E.A. 2001. African desert dust in the Caribbean atmosphere: microbiology and public health. Aerobiologia. 17, 203-213. Griffin, D .W. 2007. Atmospheric Movement of Microorganisms in Clouds of Desert Dust and Implications for Human Health. Clinical Microbiology Review. 20 (3), 459–477.

40

Griffin, D.W., Kubilay, N., Kocak, K., Gray, M.A., Borden, T.C. and Shinn, E.A. 2007. Airborne desert dust and aeromicrobiology over the Turkish Mediterranean coastline. Atmospheric Environment. 41, 4050-4062. Griffin, D.W. 2009. Desert dust storm microbiology: Issues in planetary health. In McGraw-Hill Yearbook of Science and Technology, 73-75. Griffin, D.W. 2010. Climate change and climate systems influence and control the atmospheric dispersion of desert dust: Implications for human health. In International Seminar on Nuclear War and Planetary Emergencies, 42th Session, Erice, Italy, August 19th – 24th, 2010. Editor R. Ragaini, World Scientific Publishing Co. 503-507. Griffin, D.W. 2013. The quest for extraterrestrial life: What about the viruses? Astrobiology. 13(8), 774-783. Hamasha, K., Ababneh, Z., Hamed, H., Khozima, H. 2015. Analysis of aerosol optical depth at Jordan during 2003-2012 Using Moderate Resolution Imaging Spectroradiometer (MODIS) Data. Nature Environment and Pollution Technology. 14(1): 195-202. Hamidi, M., Kavianpour, M.R. and Shao, Y. 2017. A quantitative evaluation of the 3-8 July 2009 Shamal dust storm. Aeolian Research. 24, 133-143. Hassan, S.K. and Khoder, M.I. 2017. Chemical characteristics of atmospheric PM2.5 loads during air pollution episodes in Giza, Egypt. Atmospheric Environment.150, 346-355. Herrero, B., Fombella-Blanco, M.A., Fernández-González, D. and Valencia-Barrera, R. M.1996. The role of meteorological factors in determining the annual variation of Alternaria and Cladosporium spores in the atmosphere of Palencia, 1990–1992. . International Journal of Biometeorology. l39, 139-142. Heo K.J., Lim, C.E., Kim H.B. and Lee, B.U. 2017. Effects of human activities on concentrations of culturable bioaerosols in indoor air environments. Journal of Aerosol Science 104, 58-65. Hosseini, G., Teymouri, P., Shahmoradi, B. and Maleki, A. 2015. Determination of the Concentration and composition of PM10 during the Middle Eastern dust storms in Sanandaj, Iran. Journal of Research in Health Sciences. 15(3), 182-188. Huang, J., Yu, H.; Guan, X., Wang, G. and Guo, R. 2016. Accelerated dryland expansion under climate change. Nature Climate Change . 6, 166. Jaafar, M., Baalbaki, R., Mrad, R., Daher, N., Shihadeh, A., Sioutas, C., Saliba, N.A. 2014. Dust episodes in Beirut and their effect on the chemical composition of coarse and fine particulate matter. Science of the Total Environment. 496, 75-83. Jeon, E.M, Kim, H.J., Jung, K., Kim, J.H., Kim, M.Y., Kim, Y.P. and Ka, J. 2011. Impact of Asian dust events on airborne bacterial community assessed by molecular analyses. Atmospheric Environment. 45, 4313-4321. Jones, A.M. and Harrison R.M. 2004. The effects of meteorological factors on atmospheric bioaerosol concentrations—a review. Science of the Total Environment. 326,151-180.

41

Joo, Y.S., An, S.H., Kim, O.K., Lubruth, J. and Sur, J.H. 2002. Foot-and-mouth disease eradication effors in the Repblic of Korea. Canadian Journal of Veterinary Research. 66,122-124. Kabatas, B., Unal, A., Pierce, R.B., Kindap, T. and Pozzoli, L. 2014. The contribution of Saharan dust in PM10 concentration levels in Anatolian Peninsula of Turkey. Science of the Total Environment. 488-489, 413-421. Kanatani, K.T., Hamazaki, K., Inadera, H., Sugimoto, N., Shimizu, A., Noma, H., Onishi, K., Takahashi, Y., Itazawa, T., Egawa, M., Sato, K., Go, T., Ito, I., Kurozawa, Y., Konishi, I., Adachi, Y. and Nakayama, T. Japan Environment & Children's Study Group. 2016. Effect of desert dust exposure on allergic symptoms: A natural experiment in Japan. Annals of Allergy Asthma and Immunology. 116(5), 425-430.-7. Kantarcioglu, A.S., Yucel, A. and DeHoog, G.S. 2002. Isolation of Cladosporium cladosporioides from cerebrospinal fluid. Mycoses Case Report. 45(11-12), 500-503. Kallawicha, K., Lung, S. C. C., Chuang, Y. C., Wu, C. D., Chen, T. H., Tsai, Y. J. and Chao, H.J. 2015. Spatiotemporal distributions and land-use regression models of ambient bacteria and endotoxins in the greater Taipei area. Aerosol and Air Quality Research. 15(4), 1448-1459. Karacostas, T.S., Bais, A.F., Nastos, P.T. 2017. Springer-Verlag Berlin Heidelberg Springer. Atmospheric Sciences. 415-420. Kashima, S., Yorifuji, T., Bae, S., Honda, Y., Lim, Y. H. and Hong, Y. C. 2016. Asian dust effect on cause-specific mortality in five cities across South Korea and Japan. Atmospheric Environment. 128, 20-27. Kashima, S., Yorifuji, T., Tsuda, T. and Eboshida, A. 2012. Asian dust and daily all-cause or cause-specific mortality in Western Japan. Occupational and Environmental Medicine. 69(12), 908-15 Khaniabadi, Y.O., Fanelli, R., Marco, A.D., Daryanoosh, S.M., Kloog, I., Hopke, P.K., Conti, G.O., Ferrante, M., Mohammadi, M.J., Babaei, A.A., Basiri, H. and Goudarzi, G. 2017. Hospital admissions in Iran for cardiovascular and respiratory diseases attributed to the Middle Eastern dust storms. Environmental Science and Pollution Research. 24, 1686016868. Khazaei, M., Darejeh, M., Beigi, A.M., Fahiminia, M., Azizifar, M., Karami, G., Khazaei, L. and Yousefi, N. 2016. Patterns of annual fluctuation of dust concentrations along with meteorological parameters: a case study in Qom Province, central Iran. Journal of Air Pollution and Health.1 (2), 99-110. Kellogg, C.A. and Griffin, D.W. 2006. Aerobiology and the global transport of desert dustReview. Trends in Ecology and Evolution. 21, 638–644. Kellogg, C., Griffin, D.W., Garrison, V., Peak, K., Royall, N., Smith, R. and Shinn, E. 2004. Characterization of aerosolized bacteria and fungi from desert dust events in Mali, West Africa. Aerobiologia. 20(2), 99-110.

42

Kim, H.S. and Chung, Y.S. 2010. On the sandstorms and associated airborne dustfall episodes observed at Cheongwon in Korea in 2005. Air Quality Atmosphere Health. 3 (2), 83-94. Koçak, M., Theodosi, C., Zarmpas, P., Séguret, M.J.M., Herut, B., Kallos, G., Mihalopoulos, N., Kubilay, N. and Nimmo, M. 2012. Influence of mineral dust transport on the chemical composition and physical properties of the Eastern Mediterranean aerosol. Atmospheric Environment. 57 266-277. Koçak, M., Kubilay, N. and Mihalopoulos, N. 2004. Ionic composition of lower tropospheric aerosols at a Northeastern Mediterranean site: implications regarding sources and longrange transport. Atmospheric Environment. 38, 2067-2077. Kurup, V., Shen, H and Banerjee, B. 2000. Respiratory fungal allergy. Microbes and Infection 2,1101-1110. Kwaasi, A.A. 2003. Date palm and sandstorm-borne allergens. Clinical & Experimental Allergy. 33, 419-426. Kamal, H.L., Azhaar, K.M and Ahmed, M.A. 2015. The spatial distribution of dust sources in Iraq by using satellite images. International Journal of Energy and Environment. 6(1), 2736. Lee, H., Kim, H.S., Honda, Y., Lim, Y. and Yi, S. 2013. Effect of Asian dust storms on daily mortality in seven metropolitan cities of Korea. Atmospheric Environment. 79, 510-517. Lee, S.A., Adhikari, A., Grinshpun, S.A., McKay, R., Shukla, R. and Reponen, T. 2006. Personal exposure to airborne dust and microorganisms in agricultural environments. Journal of Occupational and Environmental Hygiene3, 118–130. Leski, T.A., Malanoski, A.P., Gregory, M.J., Lin, B. and Stenger, D.A. 2011. Application of a broad-range resequencing array for detection of pathogens in desert dust samples from Kuwait and Iraq. Applied and Environmental Microbiology, 77(13), 4285–4292. Lighthart, B. and Stetzenbach, L.D. 1994. Distribution of microbial bioaerosol. In B. Lighthart & A. J. Mohr (Eds.). Atmospheric microbial aerosols. Theory and applications, 68–98. Li, Y., Lu, R., Li, W., Xie, Z. and Song, Y. 2017. Concentrations and size distributions of viable bioaerosols under various weather conditions in a typical semi-arid city of Northwest China. Journal of Aerosol Science. 106, 83–92. Lou, X., Fang, Z. and Si, G. 2012. Assessment of culturable airborne bacteria in a university campus in Hangzhou, Southeast of China. African Journal of Microbiology Research. 6, 665–673. Lyles, M.B., Fredrickson, H.L., Bednar, A.J., Fannin, H.B. and Sobecki, T.M. 2005. The chemical, biological, and mechanical characterization of airborne micro-particulates from Kuwait. Abstract, 8th Annual Force Health Protection Conference, session 2586, Louisville, KY. Ma, Y., Xiao, B., Liu, C., Zhao, Y. and Zheng, X. 2016. Association between ambient air pollution and emergency room visits for respiratory diseases in spring dust storm season in Lanzhou, China. International Journal of Environmental Research and Public Health. 13(6), 613. 43

Maleki, H., Sorooshian, A., Goudarzi, G., Nikfal, A. and Baneshi, M.M. 2016. Temporal profile of PM10 and associated health effects in one of the most polluted cities of the world (Ahvaz, Iran) between 2009 and 2014. Aeolian Research. 22, 135-140. Marzouni, M.B., Alizadeh, T., Banafsheh, M.R., Khorshiddoust, A.M., Ghozikali, M.G., Akbaripoor, S., Sharifi, R., Goudarzi, G. 2016. A comparison of health impacts assessment for PM10 during two successive years in the ambient air of Kermanshah, Iran. Atmospheric Pollution Research. 7, 768-774. Mazloomi, S., Jonidi Jafari, A., Pakzad, I. and Amarloei, A. 2017. Investigating the distribution of fungal species concentration associated with dust storms in Ilam, Iran: A Case Study. Journal of Mazandaran University of Medical Science. 27(147), 371-385 (Persian). Meng, Z. and Lu, B. 2007. Dust events as a risk factor for daily hospitalization for respiratory and cardiovascular diseases in Minqin, China. Atmospheric Environment. 41, 7048-7058. Meo, S.A., Al-Kheraiji, M.F., Alfaraj, Z.F., Alwehaibi, N.A. and Aldereihim, A. A. 2013. Respiratory and general health complaints in subjects exposed to sandstorm at Riyadh, Saudi Arabia. Pakistan Journal of Medical Sciences. 29(2), 642–646. Middleton, N., Yiallouros, P., Kleanthous, S., Kolokotroni, O., Schwartz, J., Dockery, D.W. and Koutrakis, P. 2008. A 10-year time-series analysis of respiratory and cardiovascular morbidity in Nicosia, Cyprus: the effect of short-term changes in air pollution and dust storms. Environmental health. A global access science source. 7, 39. Middleton, N. 1985. Effect of drought on dust production in the Sahel. Nature. 316(6027), 431434. Middleton, N. 1986a. Dust storms in the Middle East. Journal of Arid Environments. 10(2), 83-96. Middleton, N. 1986b. A geography of dust storms in South‐west Asia. Journal of Climatology. 6(2), 183-196.

Middleton, N. 2017. Desert dust hazards: A global review. Aeolian Research. 24, 53-63. Middleton, N. 2019. Variability and trends in dust storm frequency on decadal timescales: Climatic Drivers and Human Impacts. Geosciences. 9(6), 261 Mocali, S., Chiellini, C., Fabiani, A., Decuzzi, S., Pascale, D., Parrilli, E., Tutino, M.L., Perrin E., Bosi, E., Fondi, M., Lo Giudice, A. and Fani, R. 2017. Ecology of cold environments: new insights of bacterial metabolic adaptation through an integrated genomic-phenomic approach. Scientific Reports. 7,839–852 Moridnejad, A., Karimi, N. and Ariya, P.A. 2015. Newly desertified regions in Iraq and its surrounding areas: Significant novel sources of global dust particles. Journal of Arid Environments.116, 1-10. Morris, C.E., Sands, D.C., Bardin, M., Jaenicke, R., Vogel, B., Leyronas, C., Ariya, P.A., and Psenner, R.2011. Microbiology and atmospheric processes: research challenges concerning the impact of airborne micro-organisms on the atmosphere and climate. Biogeosciences. 8, 17–25

44

Mouli, P.C., Mohan, S.V and Reddy, S.J. 2005. Assessment of microbial (bacteria) concentrations of ambient air at semi-arid urban region: Influence of meteorological factors Applied Ecology Environment Research. 3, 139-149. NASA 2014. http://geo-pickmeup.com/atmospheric-aerosol-eddies-nasa-animated-map/ Naimabadi, A., Ghadiri, A., Idani, E., Babaei, A.A., Alavi, N., Shirmardi, M., Khodadadi, A., Marzouni M.B., Ankali, K.A., Rouhizadeh, A. and Goudarzi G. 2016. Chemical composition of PM10 and its in vitro toxicological impacts on lung cells during the Middle Eastern Dust (MED) storms in Ahvaz, Iran. Environmental Pollution. 211, 316-324 Najafi, M. S., Khoshakhllagh, F., Zamanzadeh,S. M., Shirazi, MH., Samadi, M. and Hajikhani, S. 2014. Characteristics of TSP loads during the Middle East Spring time dust storm (MESDS) in Western Iran. Arabian Journal of Geosciences. 7, 5367-5381. Nourmoradi, H., Moradnejadi, K., Moghadam, F. M., Khosravi, B., Hemati, L., Khoshniyat, R., Kazembeigi, F. 2015. The effect of dust storm on the microbial quality of ambient air in Sanandaj: A City Located in the West of Iran. Global Journal of Health Science. 7, 114– 119. Ozawa, Y., Ong, B.L. and An, S.H. 2001. Traceback systems used during recent epizootics in Asia. Revue Scientifique Technique. 20,605-613. Ozkara, A., Ocak, I., Korcan, S.E., Konuk, M. 2007. Determination of fungal air spora in Afyonkarahisar, Turkey. Mycotaxon. 102, 199-202. Polymenakou, P.N., Mandalakis, M., Stephanou, E.G. and Tselepides, A. 2008. Particle size distribution of airborne microorganisms and pathogens during an Intense African dust event in the eastern Mediterranean. Environmental Health Perspectives. 116(3), 292-6. Popova, N.A., Nikolaev, Y.A., Tourova, TP., Lysenko, AM., Osipov, GA., Verkhovtseva, N. and Panikov, N.S. (2002). Geobacillus uralicus, a new species of thermophilic bacteria. Microbiology. 71, 335-341. Perez L and Tobías A. 2012. Saharan dust, particulate matter and cause-specific mortality: A case–crossover study in Barcelona (Spain). Environment International. 48, 150–155. Perez, L., Tobias A., Künzli, N., Lysenko, A.M., Osipov, G.A., Verkhovtseva, N.V. and Panikov, N.S.2008. Coarse particles from Saharan dust and daily mortality. Epidemiology. 19(6), 800-7. Prospero, J.M., Ginoux, P., Torres, O., Nicholson, S.E. and Gill, T.E. 2002. Environmental characterization of global sources of atmospheric soil dust identified with the Nimbus 7 Total Ozone Mapping Spectrometer (TOMS) absorbing aerosol product. Reviews of Geophysics 40, 2qGx Prospero, J.M., Blades, E., Mathison, G. and Naidu, R. 2005. Interhemispheric transport of viable fungi and bacteria from Africa to the Caribbean with soil dust. Aerobiologia. 21, 1– 19. Pu, B. and Ginoux, P. 2017. Projection of American dustiness in the late 21st century due to climate change. 7, 5553.

45

Rashki, A., Eriksson , P. G., Rautenbach, C.J., Kaskaoutis, D.G., Grote, W. and Dykstra, J. 2013. Assessment of chemical and mineralogical characteristics of airborne dust in the Sistan region, Iran. Chemosphere. 90, 227-236. Rashki, A., Kaskaoutis, D.G., Francois, P., Kosmopoulos, P.G. and Legrand, M., 2015. Duststorm dynamics over Sistan region, Iran: Seasonality, transport characteristics and affected areas. Aeolian Research, 16,35-48. Rezazadeh, M., Irannejad P. and Shao, Y. 2013. Climatology of the Middle East dust events. Aeolian Research. 10, 103-109. Sabariego, S., Díaz de la Guardia, C., Alba, F. 2000. The effect of meteorological factors on the daily variation of airborne fungal spores in Granada (southern Spain). International Journal of Biometeorology. 44(1), 1–5. Saeed, T.M., Al-Dashti, H. and Spyrou, C. 2014. Aerosol’s optical and physical characteristics and direct radiative forcing during a shamal dust storm, a case study. Atmospheric Chemistry and Physics. 14, 3751-3769. Sahebzadeh, B., Shabani-Goraji, K., Shoaei, Z., Afshari, M. 2019. Statistical study of eolian sediment distribution risk in human ecosystems on the health of respiratory system and the eyes of inhabitants of Sistan, East Iran. Arabian Journal of Geosciences. 12, 227. Sakamoto, K. and Yoshida, K. 2002. Recent outbreaks of foot and mouth disease in countries East Asia. Revue Scientifique Technique. 21,459-463. Saliba, N.A., Kouyoumdjian, H. and Roumié M., 2007. Effect of local and long-range transport emissions on the elemental composition of PM10–2.5 and PM2.5 in Beirut. Atmospheric Environment. 41 6497-6509. Samoli, E., Kougea, E., Kassomenos, P., 2011. Does the presence of desert dust modify the effect of PM10 on mortality in Athens, Greece? Science of the Total Environment. 409, 2049–2054. Sandstrom, T. and Forsberg, B. 2008. Desert dust: an unrecognized source of dangerous air pollution? Epidemiology. 19 (6), 808–809. Shahsavani, A., Naddafi, K., Jafarzade Haghighifard, N., Mesdaghinia, A., Yunesian, M., Nabizadeh, R., Arahami, M., Sowlat, M.H., Yarahmadi, M., Saki, H., Alimohamadi, M., Nazmara, S., Motevalian, SA., Goudarzi, G.2012. The evaluation of PM10, PM2.5, and PM1 concentrations during the Middle Eastern Dust (MED) events in Ahvaz, Iran, from April through September 2010. Journal of Arid Environments. 77 (1), 72-83. Shaka, H. and Saliba, N.A. 2004. Concentration measurements and chemical composition of PM10-2.5 and PM2.5 at a coastal site in Beirut, Lebanon. Atmospheric Environment. 38 523531. Sissakian, V.K., Al-Ansari, N, and Knutsson S. 2013. Sand and dust storm events in Iraq Natural Science. 5(10), 1084-1094. Smets, W., Moretti, S., Denys, S., Lebeer, S. 2016. Airborne bacteria in the atmosphere: Presence, purpose, and potential. Atmospheric Environment. 139, 214-221.

46

Smith, D.J., Griffin, D.W., McPeters, R.D., Ward, P.D. and Schuerger, A.C., 2011. Microbial survival in the stratosphere and implications for global dispersal. Aerobiologia. 27(4), 319332. Smith, D.J., Ravichandar, J.D., Jain, S., Griffin, D.W., Yu, H., Tan, Q., Thissen, J., Lusby, T., Nicoll, P., Shedler, S., Martinez, P., Osario, A., Lechniak,J., Choi, S., Sabino, K., Iverson, K., Chan, L., Jaing, C. and McGrath, J. 2018. Airborne bacteria in Earth’s lower stratosphere resemble taxa detected in the troposphere: Results from a new NASA Aircraft Bioaerosol Collector (ABC). Frontiers in Microbiology. 9, 1752 Soleimani, Z., Goudarzi, G., Naddafi, K., Sadeghinejad, B., Latifi, S. M., Parhizgari, N., Shahsavani, A.2013. Determination of culturable indoor airborne fungi during normal and dust event days in Ahvaz, Iran. Aerobiologia. 29(2), 279–290. Soleimani, Z., Parhizgari, N., Dehdari Rad, H., Akhoond, M.R., Kermani, M., Marzouni, M.B., Goudarzi, H., & Goudarzi, G. 2015. Normal and dusty day’s comparison of culturable indoor airborne bacteria in Ahvaz, Iran. Aerobiologia. 31, 127-141. Soleimani, Z., Goudarzi,G., Sorooshian, A., Marzouni, M.B., Maleki, H. 2016. Impact of Middle Eastern dust storms on indoor and outdoor composition of bioaerosol. Atmospheric Environment. 138 135-143. Soleimani, Z., Darvishi Boloorani, A., Khalifeh, R., Griffin, D.W., & Mesdaghinia, A. 2019. Short-term effects of ambient air pollution and cardiovascular events in Shiraz, Iran, 2009 to 2015. Environmental Science and Pollution Research, 26, 6359-6367. Soleimani, Z., Darvishi Boloorani, A., Khalifeh, R., Teymouri, P., Mesdaghinia, A., Griffin, D.W.2019. Air pollution and respiratory hospital admissions in Shiraz, Iran, 2009 to 2015. Atmospheric Environment. 209, 233-239. Sprigg, W.A., 2016. Dust storms, human health and a global early warning system. In: extreme weather, health, and communities. Springer International Publishing.59–87. Taheri Shahraiyni H., Karimi, K., Habibi Nokhandan, M., Moghadas, N.H. 2015. Monitoring of dust storm and estimation of aerosol concentration in the Middle East using remotely sensed images. Arabian Journal of Geosciences. 8, 2095-2110. Tang, J.W. 2009. The effect of environmental parameters on the survival of airborne infectious agents. Journal of the Royal Society Interface. 6, S737–S746. Tao, Y., An, X., Sun,Z., Hou, Q., Wang ,Y. 2012. Association between dust weather and number of admissions for patients with respiratory diseases in spring in Lanzhou. Science of the Total Environment. 423, 8–11. Tarigan, Y.G., Chen, R.Y., Lin, H.C., Jung, C.Y., Kallawicha, K., Chang, T.P., Chao, H.J. 2017. Fungal bioaerosol exposure and its effects on the health of mushroom and vegetable farm workers in Taiwan. Aerosol and Air Quality Research, 17(8), 2064-2075

47

Teigell-Perez, N., Gonzalez-Martin, C., Valladares, B., Smith, D.J. and Griffin, D.W. 2019. Virus-like particle production in atmospheric eubacteria isolates. Atmosphere. 10, 417 Thalib, L. and Al-Taiar, A. 2012. Dust storms and the risk of asthma admissions to hospitals in Kuwait. Science of the Total Environment.433, 347-351. Thilsing, T., Madsen, A.M., Basinas, I., Schlunssen, V., Tendal, K. and Baelum, J. 2015. Dust, endotoxin, fungi, and bacteria exposure as determined by work task, season, and type of plant in a flower greenhouse. Annals of Occupational Hygiene. 59, 142–157. Thompson, L.G. 2001. Stable isotopes and their relationship to temperature as recorded in lowlatitude ice cores. In: Gerhard, L.C., W.E. Harrison and B.M. Hanson, eds. Geological perspectives of global climate change. Tulsa: The American Association of Petroleum Geologists, 99-119 Tobías, A., Pérez, L., Díaz, J., Linares, C., Pey, J., Alastruey, A., Querol, X. 2011. Short-term effects of particulate matter on total mortality during Saharan dust outbreaks: A casecrossover analysis in Madrid (Spain). Science of the Total Environment (412–413): 386389. Trianti, S., Samoli, E., Rodopoulou, S., Katsouyanni, K., Papiris, S.A., and Karakatsani, A. 2017. Desert dust outbreaks and respiratory morbidity in Athens, Greece. Environmental Health. 16(1), 72. Troutt, C. and Levetin, E. 2002. Correlation of spring spore concentrations and meteorological conditions in Tulsa, Oklahoma. International Journal of Biometeorology. 45, 64-74. Uduma, A.U and Jimoh W.L.O. 2013. High incidence of asthma, bronchitis, pneumonia and sinusitis in Kano State, North West Nigeria during Saharan dust events. American Journal of Environment. Energy and Power Research .1 (8), 174 – 185. WAO, World Atlas of Aeroallergens: Middle East http://www.worldallergy.org/resources/worldatlas-of-aeroallergens/middle-east. Whitman, W.B., Coleman, D.C., Wiebe, W. J. 1998. Prokaryotes: the unseen majority. Proceedings of the National Academy of Sciences. USA .95, 6578-6583. Yu, H.L and Chien, L.C. 2012. Asian dust storm elevates children’s respiratory health risks: A spatiotemporal analysis of children’s clinic visits across Taipei (Taiwan). PLOS One. 7 (7), 41317. Yu H.L, Yang C.H and Chien L.C. 2013. Spatial vulnerability under extreme events: A case of Asian dust storm's effects on children's respiratory health. Environment International. 54, 35–44. Zakey, A. S., Abdelwahab, M .M. and Makar P.A. 2004. Atmospheric turbidity over Egypt. Atmospheric Environment. 38, 1579-1591. Zauli Sajani, S., Miglio, R., Bonasoni, P., Cristofanelli P, Marinoni A, Sartini C, Goldoni CA, De Girolamo G, Lauriola P. 2011. Saharan dust and daily mortality in EmiliaRomagna (Italy). Occupational and Environmental Medicine. 68(6), 446-51.

48

Zhang, Q., Zhang, J., Yang, Z., Zhang, Y., Meng, Z. 2013. Impact of PM 2.5 derived from dust events on daily outpatient numbers for respiratory and cardiovascular diseases in Wuwei, China. Procedia Environmental Sciences 18, 290-298. Zheng, Y., Zhao, T., Che, H., Liu, Y., Han, Y., Liu, C., Xiong, J., Liu, J., & Zhou, Y. 2016. A 20-year simulated climatology of global dust aerosol deposition. Science of the Total Environment, 557, 861-868. Zhong, X., Qi, J., Li, H., Dong, L., Gao, D. 2016. Seasonal distribution of microbial activity in bioaerosols in the outdoor environment of the Qingdao coastal region. Atmospheric Environment. 140, 506-513.

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Highlights First review study of its kind to present on dust storms and their impact health and bioaerosols in the Middle East. The Middle East has heavy PM10 loads that are due to dust storms. A review of dust event studies, their particulate matter concentrations, their points of origins, seasonality and movement routes have been summarized in this paper. Aerobiology: collection, concentration and identification of microorganisms. The influence of environmental factors on the viability of microorganisms in the atmosphere and the health effects of bioaerosol (bacteria, fungi) exposure.

Declaration of Interest Statement - We, all named authors, have seen and agreed to the submitted version of the paper; that all who are included in the acknowledgements section, or as providers of personal communications, have agreed to those inclusions; and that the material is original, unpublished and has not been submitted elsewhere. - We do not have any material which has been published elsewhere and is contained in a contribution to the Journal. We have nothing to declare in this category. - We have no conflict of interest. - This research has funded by research deputy of Tehran University of Medical Sciences. - We are not submitting randomized controlled trial, so that we have nothing to declare in this category. - There was no need for ethical approval for this study.