Status and Trend of the Main Allergenic Pollen Grains and Alternaria Spores in the City of Rome (2003-2019)
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sustainability Article Status and Trend of the Main Allergenic Pollen Grains and Alternaria Spores in the City of Rome (2003–2019) Alessandro Di Menno di Bucchianico 1,2, * , Raffaela Gaddi 1 , Maria Antonia Brighetti 2 , Denise De Franco 2 , Annarosa Miraglia 2 and Alessandro Travaglini 2 1 ISPRA—Italian Institute for Environmental Protection and Research, Via Brancati 48, 00144 Rome, Italy 2 PhD Program in Evolutionary Biology and Ecology, Department of Biology, University of Rome Tor Vergata, 00133 Rome, Italy * Correspondence: alessandro.dimenno@isprambiente.it Abstract: Today a large part of the European population is exposed to levels of air pollution exceeding the standards recommended by the World Health Organization. Moreover, air pollution and the seasonal emission of allergenic pollen are progressively affecting human health and can cause severe allergic reactions, particularly when air pollution combines with pollen allergen peaks. Unlike atmospheric pollutants of anthropogenic origin, pollen sources have a pulsating trend that leads to high values in the flowering period and values close to, or equal to, zero in the rest of the year. This aspect makes essential the definition of data coverage standards for the main allergenic taxa. For air quality assessment detailed classification criteria for monitoring stations are defined by international standards, not the same from the European Standards for the Sampling and analysis of airborne pollen grains and fungal spores. This paper describes the status and the air concentration trends of the main allergenic pollen and the Alternaria spore measured in Rome from 2003 to 2019 by the Aerobiological Monitoring Center of Tor Vergata (Rome) and calculated by the Seasonal Citation: Di Menno di Bucchianico, Kendall test with the open-source OpenAir R package. The analysis was carried out on the daily A.; Gaddi, R.; Brighetti, M.A.; De concentrations of the most widespread allergenic taxa in Italy: Asteraceae, Betulaceae, Corylaceae, Franco, D.; Miraglia, A.; Travaglini, A. Cupressaceae/Taxaceae, Poaceae, Oleaceae, Urticaceae and the Alternaria spores. Status and Trend of the Main Allergenic Pollen Grains and Keywords: pollen; atmospheric pollution; urban areas; allergy; pollen concentration Alternaria Spores in the City of Rome (2003–2019). Sustainability 2023, 15, 6150. https://doi.org/10.3390/ su15076150 1. Introduction Academic Editors: Assunta The lower troposphere of temperate zones is often rich in airborne pollen, this is Florenzano, Eleonora Clò, Gabriel particularly true in Italy due to the remarkable plant biodiversity that characterizes this Servera-Vives and Anna Maria territory. In every season we find blooms of anemophilous species whose pollen and Mercuri spores, often allergenic, are released in large quantities and are dispersed in the air. This Received: 30 December 2022 phenomenon is significantly reduced only in the coldest winter periods. Throughout the Revised: 19 March 2023 developed world, pollinosis, i.e., pollen allergies, are continuously increasing and are Accepted: 21 March 2023 increasing more in urban areas also due to the synergistic effect, on human health, between Published: 3 April 2023 the allergens present in pollen grains and atmospheric pollution [1–6]. Allergic diseases affect over a billion people worldwide [7] and the role of pollen in the pathogenesis of these diseases is now well established. In fact allergic diseases, such as asthma and rhinitis, affect from 5 to 30% of the inhabitants of industrialized countries [8]. Copyright: © 2023 by the authors. To date, however, it is not fully understood the mechanism of the interaction between Licensee MDPI, Basel, Switzerland. pollen allergens and air pollutants and further research will be needed to clarify the process This article is an open access article by which biological pollutants can cause symptoms in exposed population. distributed under the terms and Pollen and allergies are a recurring theme every spring. In fact, every year, in the conditions of the Creative Commons different seasons, periodic environmental alarms are raised, such as high levels of PM10 Attribution (CC BY) license (https:// in winter or ozone in summer. Nevertheless in Italy the allergenic pollen season is spread creativecommons.org/licenses/by/ from January (Cupressaceae) to November (Ambrosia), (see ahead Table 1). 4.0/). Sustainability 2023, 15, 6150. https://doi.org/10.3390/su15076150 https://www.mdpi.com/journal/sustainability
Sustainability 2023, 15, 6150 2 of 15 Table 1. Average pollen and sporulation seasons and allergenicity for main allergenic taxa in Italy (X: moderate, XX: medium, XXX: intense). Betulaceae Asteraceae Corylaceae Cupressaceae/Taxaceae Allergenicity Very High Allergenicity Very High Allergenicity Very High Allergenicity Very High Jan. Jan. Jan. XX Jan. XX Feb. X Feb. Feb. XXX Feb. XXX Mar. XX Mar. Mar. X Mar. XXX Pollen Calendar (Italy) Pollen Calendar (Italy) Pollen Calendar (Italy) Pollen Calendar (Italy) Apr. XX Apr. Apr. XXX Apr. XX May X May May X May X Jun. Jun. Jun. Jun. Jul. Jul. X Jul. Jul. Aug. Aug. XXX Aug. Aug. Sep. Sep. XX Sep. Sep. Oct. Oct. Oct. Oct. Nov. Nov. Nov. Nov. Dec. Dec. Dec. X Dec. X Poaceae Oleaceae Urticaceae Alternaria spore Allergenicity Very high Allergenicity Very high Allergenicity Very high Allergenicity Very high Jan. Jan. Jan. Jan. Feb. Feb. XX Feb. Feb. Mar. X Mar. XXX Mar. X Mar. Sporulation Calendar (Italy) Pollen Calendar (Italy) Pollen Calendar (Italy) Pollen Calendar (Italy) Apr. XX Apr. XX Apr. XXX Apr. May XXX May XXX May XXX May X Jun. XX Jun. XX Jun. XX Jun. XX Jul. XX Jul. Jul. XX Jul. XX Aug. X Aug. Aug. XXX Aug. XXX Sep. X Sep. Sep. XXX Sep. XXX Oct. X Oct. Oct. X Oct. XX Nov. Nov. Nov. Nov. X Dec. Dec. Dec. Dec. In recent years, the recorded cases of pollen allergies in urban centers of Italy and Europe have been increasing [5,8]. This evidence cannot be explained only by genetic factors but the trend of allergenic pollen concentrations in the air must be investigated which, linked to green management and rapid urbanization, increases the number of people exposed to air pollution. In recent years, the interest of scientific research for the monitoring of pollen, spores and other bioaerosols has increased due to the growing awareness of the importance of respiratory diseases. Furthermore, the role of climate change on the future worldwide distribution of bioaerosols and consequently on human health has influenced the growth of interest in this topic. A review conducted in Scopus has in fact highlighted that the number of publica- tions containing terms such as “pollen allergies” and “pollen predictions” is constantly increasing [9]. It is therefore increasingly clear that aerobiological monitoring is an integral part of the assessment of air quality, in line with a significant number of epidemiological studies
Sustainability 2023, 15, x FOR PEER REVIEW 3 of 15 Sustainability 2023, 15, 6150 3 of 15 which show how the interaction between air pollutants and allergens can increase the risk which show of disease how and thethe interactionofbetween aggravation symptoms air pollutants [10]. and allergens can increase the risk of disease and the aggravation of symptoms [10]. Aerobiology research has been working for years for the monitoring and assessment of airAerobiology quality linked research has been to pollutants working for years of anthropogenic for and origin, the monitoring and assessment at the same time also carries of air quality linked to pollutants of anthropogenic origin, and out the analysis and evaluation of allergenic pollen sampled by Aerobiological at the sameMonitoring time also carries Networks. out the analysis and evaluation of allergenic pollen sampled by Aerobiological Monitoring The issuesNetworks. of interest to the scientific community and citizens are many and strongly The issues of linked to each other, interest to the to in addition scientific community the relationship and citizens between pollen are andmany human and strongly health, the linked to each other, in addition to the relationship between pollen and relationship between pollen and climate change will be deepened in the near future and human health, the relationship between pollen and climate change will be deepened in the near future and a a more modern, and informed, design will be supported. The aim must not be simply the more modern, and informed, design will be supported. The aim must not be simply the reduction of allergic reactions, but more generally to contribute to the citizen s well-being reduction of allergic reactions, but more generally to contribute to the citizen’s well-being and awareness growth. and awareness growth. The purpose of this study was to evaluate the presence of monotonic trends of air The purpose of this study was to evaluate the presence of monotonic trends of air concentration of the main allergenic taxa in the city of Rome from 2003 to 2019: Asteraceae concentration of the main allergenic taxa in the city of Rome from 2003 to 2019: Asteraceae (a family that include the Ambrosia and Artemisia genera), Betulaceae (main genera: Alnus (a family that include the Ambrosia and Artemisia genera), Betulaceae (main genera: Alnus and Betula), Corylaceae (which includes the genera Carpinus, Corylus and Ostrya), Cupres- and Betula), Corylaceae (which includes the genera Carpinus, Corylus and Ostrya), Cupres- saceae/Taxaceae (counted together in aerobiological monitoring), Poaceae (which includes saceae/Taxaceae (counted together in aerobiological monitoring), Poaceae (which includes many herbaceous allergenic plants widespread in Italy), Oleaceae (main genera: Fraxinus many herbaceous allergenic plants widespread in Italy), Oleaceae (main genera: Fraxinus and Olea), and Olea), Urticaceae Urticaceae (main (main genera: genera: Parietaria Parietaria and Urtica) and and Urtica) and the the Alternaria Alternaria spore spore [11–17] [11–17] and chapter S1 in Supplementary and chapter S1 in Supplementary Materials. Materials. The assessment The assessment of of aa possible possible presence presence of of an an increasing increasing or or decreasing decreasing trend trend of of specific specific allergenic taxa allergenic taxa can can provide provide aa useful useful tool tool for for interpreting interpreting symptoms symptomsin inatopic atopicsubjects. subjects. 2. Materials 2. and Methods Materials and Methods homogeneous pollen This paper compares homogeneous pollen concentration concentration time time series of data collected in Rome and describes the status and trend of the main allergenic taxa present in the study during the area during the years years from from 2003 2003 to to 2019 2019 [18–22]. [18–22]. Pollen samples were collected and measured Pollen samples were collected and measured inin two two sampling sampling sites sites by by thethe Aerobio- Aerobiologi- logical cal monitoring monitoring center center of Vergata of Tor Tor Vergata (see (see Figure Figure 1). 1). 1. Aerobiological Figure 1. Aerobiological Monitoring Monitoring stations stations of of Tor Vergata center center (red (red line: line: Great Ring Road of Rome; blue line: Tiber river). The spatial and temporal comparability of the data obtained in the two sites was calculated through the Pearson correlation analysis of daily concentrations.
Sustainability 2023, 15, 6150 4 of 15 Temporal trends of pollen and spores were realized using the Seasonal Kendall test in R software (R version 4.1.3, developed by R Core Team) [23,24]. Statistical analysis allowed to highlight the trends in the levels of allergenic species and how the distribution of peaks changes over time in order to link them to meteorological parameters and the flowering calendar. The seasonally adjusted Kendall test is a non-parametric statistical hypothesis test aimed to evaluate the existence of a trend or an increasing or decreasing monotonous trend given a sufficiently large sample of data. The first version of the test proposed by Mann in 1945 [25] extended the analysis of the significance of the Kendall τ correlation coefficient [26]—a test developed to evaluate the association between any two variables regardless of the distribution of the data—if one of the variables was time. The Mann-Kendall test was modified to take into account the effects due to season- ality; the latter test is known as Seasonal Kendall Test (SK) or Kendall test corrected for seasonality [27,28]. It has been shown that among the various parametric and non-parametric tests avail- able for trend analysis, the SK is among those that obtain the best performance, compared to other tests, evaluated through the use of fictitious time series [29]. It is able to predict the existence of a statistically significant trend by keeping the error percentage below the predetermined value, and at the same time, to identify weak statistically significant trends where actually present in the fictitious series. As this is a non-parametric test, it is independent of the hypothesis of normality of the data. This method is robust in case of anomalous (outliers) and missing data and characterized by a relatively simple implementation [30]. Furthermore, when applied to historical series of air pollution data, identifying and removing the seasonal component (seasonal adjustment) can improve the estimation of background trends, reducing the uncertainty associated with the estimate [31]. In any case, trend analysis cannot disregard the availability of sufficiently long time series, in order to reduce the influence of years with atypical weather conditions that can mask an existent trend. It has been shown that the uncertainty in determining the existence of a statistically significant trend in a series of air quality data increases exponentially with decreasing length of the series. To be able to appreciate very small decreasing or increasing trends, it is necessary to have datasets that are approximately 15 years long. With shorter series the trend becomes appreciable if it is more significant but the series must be at least seven years long. The normalization of data for the effects of meteorology allows to reduce the uncertainty associated with the estimate and therefore to appreciate the existence of a trend of the same order of magnitude starting from relatively less extensive data series [32]. 2.1. The Monitoring Stations The pollen and spore concentration data for Rome were provided by the Aerobiological Monitoring Center of the Tor Vergata University of Rome (Station code: RM5). The Tor Vergata Aerobiological Monitoring Center began its activity in 1996. The volumetric sampler VPPS 2000, located approximately 15 m above the ground on the roof of the Faculty of Mathematical, Physical and Natural Sciences, was installed a few years after the purchase of the meteorological station of the Botanical Garden (1991). At the same time, a cognitive study of the flora of the Campus territory was carried out, before its transformation. Soon the activity of the monitoring center was made available to the doctors of the university and of the city. In 1999 the Center installed another monitoring station, 18 m above the ground on the roof of the S. Pietro Fatebenefratelli Hospital research center (Station code: RM6) in the northern zone of Rome.
Sustainability 2023, 15, x FOR PEER REVIEW 5 of 15 Sustainability 2023, 15, 6150 5 of 15 In 1999 the Center installed another monitoring station, 18 m above the ground on the roof of the S. Pietro Fatebenefratelli Hospital research center (Station code: RM6) in the northern zone of Rome. Around Around the stations(see the two stations (seeFigure Figure2)2)the the vegetational vegetational picture picture is heterogeneous: is heterogeneous: ev- evergreen anddeciduous ergreen and deciduoussclerophyllous sclerophyllouswoods woodson onthe theright rightbank bankofof the the Tiber Tiber River, semi- semi- natural naturalmeadows meadowstowards towardsthetheeastern easternpart partofof thethe city, upup city, to deciduous to deciduousbroadleaf woods broadleaf on woods the Alban hills and the Simbruini mountains [33]. on the Alban hills and the Simbruini mountains [33]. Figure2.2. Tor Figure TorVergata VergataCenter Center(RM5) (RM5)and andS.S.Pietro PietroHospital Hospital(RM6), (RM6),Rome Rome(Source: (Source:Department Department of of Biology, University of Tor Vergata). Biology, University of Tor Vergata). 2.2. 2.2.Instrumental InstrumentalDescription Description For Forthethepollen pollenmonitoring monitoringaavolumetric volumetricsampler-type sampler-typeHirst Hirst[34], [34],recommended recommendedby bythe the International InternationalBiological BiologicalProgram Program[35],[35],Model Model20002000VPPS VPPSLanzoni Lanzoni[36], [36],was wasused. used. The TheHirst Hirstdevice devicesamples samples ambient ambient air air by by aavolumetric volumetric suction suction system, system, particles particles con- con- tained in tained in the sampled air are deposited by impaction on a sampling surface air are deposited by impaction on a sampling surface and then ex- and then examined amined with withananoptical opticalmicroscope microscopein inorder order to to identify identify and count the pollen pollen and and fungal fungal spores sporesperperarea. area. The The data data acquisition acquisition waswas made made following following the the procedure procedure described described inin the the UNI UNI EN EN Standard Standard 16868:2019 16868:2019 [37] [37] and and reported reported in in the the Management Management and and quality quality manual manual of of the the R.I.M.A. Italian Monitoring Network in Aerobiology (Manuale di gestione R.I.M.A. Italian Monitoring Network in Aerobiology (Manuale di gestione e qualità della e qualità della Rete ReteItaliana ItalianadidiMonitoraggio Monitoraggioin inAerobiologia) Aerobiologia)[38].[38]. The The pollen and spores data of the pollen and spores data of the considered considered taxataxa were were expressed expressed asas daily daily concentra- concentra- tion in Pollen/m 3 (P/m3 ) or Spore/m3 [39]. tion in Pollen/m3 (P/m3) or Spore/m3 [39]. The TheHirst Hirstdevice devicesamples samplesambient ambientair airby byaavolumetric volumetriclow-volume low-volumesystem system[10 [10L/min] L/min] and and pollen grains are collected on a moving acceptor surface. Samples are identifiedand pollen grains are collected on a moving acceptor surface. Samples are identified and counted countedby byoptical opticalmicroscopy microscopy[37,40–43]. [37,40–43]. 3. Results and Discussion 3. Results and Discussion 3.1. Pollen Time Series in Rome 3.1. Pollen Time Series in Rome A first assessment that can be extrapolated from the analysis of the data from 2003 to 2019A first assessment concerns that can be extrapolated the predominant allergenic taxa from in the the analysis of the study area. Indata this from sense,2003 both to 2019 concerns the predominant allergenic taxa in the study area. In considered monitoring stations showed the analyzed taxa in the same order of presence this sense, both con- sidered even monitoring if with differentstations showed quantity, due tothetheanalyzed taxa in the same specific characteristics order of the of presence sampling sites.even if with Thedifferent allergenicquantity, due to the the taxon presenting specific characteristics highest of the sampling average concentration in thesites. air in Rome area isThe allergenic taxon presenting Cupressaceae/Taxaceae (whose thepollen highest average grains are concentration counted together) in the air inrespec- with, Rome area isfor tively Cupressaceae/Taxaceae stations RM5 and RM6, (whose 36%pollen and 63% grains are average of the counted total together) with, respec- concentration for tively for stations RM5 and RM6, 36% and 63% of the average total concentration the entire period. Second, for average air concentration, Urticaceae with, respectively for for the entire period. Second, for average air concentration, Urticaceae with, respectively stations RM5 and RM6, 27% and 18% of the total; third taxon, for average presence, Poaceae for sta- tions respectively with, RM5 and RM6, for 27% and RM5 stations 18% ofand theRM6, total;16% thirdandtaxon, 8% for average of the total; presence, Poaceae fourth taxon, for with, respectively average for stations presence, Oleaceae RM5 with, and RM6,for respectively 16% and 8% stations of the RM5 andtotal; RM6,fourth 10% andtaxon,5% for of average the total, presence, followed by Oleaceae with, respectively Corylaceae, Betulaceae and, for stations RM5 and RM6, lastly, Asteraceae 10%than with less and 1% 5%at of the total, both followed stations (see the bypie Corylaceae, Betulaceae charts in Figure 3). and, lastly, Asteraceae with less than 1% at both stations (see the pie charts in Figure 3).
entire period. Second, for average air concentration, Urticaceae with, respectively for tions RM5 and RM6, 27% and 18% of the total; third taxon, for average presence, Poa with, respectively for stations RM5 and RM6, 16% and 8% of the total; fourth taxon average presence, Oleaceae with, respectively for stations RM5 and RM6, 10% and 5 Sustainability 2023, 15, 6150 the total, followed by Corylaceae, Betulaceae and, lastly, Asteraceae with6 ofless 15 than 1 both stations (see the pie charts in Figure 3). ROME RM5 2003-2019 Sustainability 2023, 15, x FOR PEER REVIEW 7 BETULACEAE RM5 ASTERACEAE RM5 CORYLACEAE RM5 CUPRESSACEAE/TAXACEAE RM5 POACEAE RM5 OLEACEAE RM5 URTICACEAE RM5 ROME RM6 2003-2019 BETULACEAE RM6 ASTERACEAE RM6 CORYLACEAE RM6 CUPRESSACEAE/TAXACEAE RM6 POACEAE RM6 OLEACEAE RM6 URTICACEAE RM6 Figure Figure 3. 3. Average Average pollen pollen concentration concentration in the in the two two aerobiological aerobiological monitoringmonitoring stations, RM5stations, (top) andRM5 (top RM6(bottom), RM6 (bottom), for for the period the period 2003–2019. 2003–2019. The simple graphic evaluation of the time series is the first step in the evaluation The simple graphic evaluation of the time series is the first step in the evaluati of the possible variations over time of the concentrations of a pollutant in the air (see the possible Figure 4). Whatvariations overfrom can be deduced time ofrepresentation this the concentrations ofconcentration is that the a pollutant in theare levels air (see F 4). What clearly basedcan be different on the deduced from pollen this [44,45], seasons representation is that characteristic the of each concentration taxon, which are level clearly regularly repeated based oninthe different pollen the considered seasons [44,45], characteristic of each taxon, w years (2003–2019). are For all the taxa, repeated the temporal regularly in thecorrespondence between considered years the peak concentrations recorded (2003–2019). in the sampling stations throughout the period is very good, which indicates that the two sampling sites respond to the same meteorological and climatic conditions. On the other hand, some evident differences emerge in the recorded concentration values, this can be explained by the botanical biodiversity that characterizes the neighbourhoods of the two sampling points [46].
Sustainability 2023, 15, x FOR PEER REVIEW 7 of 15 Sustainability 2023, 15, 6150 7 of 15 Figure 4. Daily pollen and spore concentration from Tor Vergata Center (RM5, in red) and S. Pietro Figure 4. Daily pollen and spore concentration from Tor Vergata Center (RM5, in red) and S. Pietro Hospital (RM6, in green) in the period 2003–2019. Hospital (RM6, in green) in the period 2003–2019. From the mere evaluation of these time series, however, it is not possible to understand For allinthe whether, thetaxa, period the temporalthe considered, correspondence between concentration has the trend, significant peak but concentrations only obtain rec- indications orded on the phase in the sampling correlation stations between the throughout the concentration period is very values good,detected whichover time. that indicates The calculation of the correlation matrix between the variables observed for the two sampling sites respond to the same meteorological and climatic conditions. On the period the other hand, some evident differences emerge in the recorded concentration values, this can be explained by the botanical biodiversity that characterizes the neighbourhoods of the two sampling points [46]. From the mere evaluation of these time series, however, it is not possible to under-
Sustainability 2023, 15, 6150 8 of 15 2003–2019 (expressed as Pearson’s coefficient of the pairs of daily averages) revealed that all the taxa showed statistically significant correlations (p < 0.001) between the two sampling sites (Tor Vergata Center, RM5 and S. Pietro Hospital RM6), this indicates a good spatial representativeness for the urban area of Rome. This indicates a good spatial representativeness of the two sites considered for the urban area of Rome [see Table S1 and Figure S1 in Supplementary Materials]. In contrast, the different taxa, both in the same station and between the two sam- pling sites, showed a minimal correlation, with the exception of the pairs: Cupressaceae/ Taxaceae—Betulaceae; Corylaceae—Urticaceae; Poaceae—Oleaceae and Oleaceae—Urticaceae. This result can be mainly attributed to the different extension and timing of the pollen sea- sons, outside of which the emissions of pollen grains into the air tends to zero. The pairs of taxa showing a greater correlation in daily values are those with more overlapping pollen seasons (see Table 2), where atmospheric stability variations represent a significant driver of concentrations in the air as for other atmospheric contaminants. Table 2. Kendall trend test results for the main allergenic taxa in Rome (2003–2019). Kendall Trend Test Results (2003–2019) Statistical Significance Taxon Station Code Station Name P Stars p Dy (P m3 y−1 ) Significance Trend RM5 Roma Tor Vergata 0.31 −0.00029 No Decreasing Betulaceae RM6 Roma S. Pietro * 0.03 0.00234 Yes Increasing RM5 Roma Tor Vergata *** 0.00 −0.01673 Yes Decreasing Asteraceae RM6 Roma S. Pietro ** 0.00 −0.01587 Yes Decreasing RM5 Roma Tor Vergata 0.76 0.00030 No Increasing Corylaceae RM6 Roma S. Pietro * 0.02 −0.00804 Yes Decreasing RM5 Roma Tor Vergata * 0.03 −0.06714 Yes Decreasing Cupressaceae/Taxaceae RM6 Roma S. Pietro *** 0.00 −0.33262 Yes Decreasing RM5 Roma Tor Vergata 0.92 0.00163 No Increasing Poaceae RM6 Roma S. Pietro 0.10 −0.04692 No Decreasing RM5 Roma Tor Vergata 0.17 −0.00711 No Decreasing Oleaceae RM6 Roma S. Pietro *** 0 −0.04490 Yes Decreasing RM5 Roma Tor Vergata + 0.10 0.26481 No Increasing Urticaceae RM6 Roma S. Pietro 0.17 −0.22694 No Decreasing RM5 Roma Tor Vergata *** 0 −0.52906 Yes Decreasing Alternaria RM6 Roma S. Pietro *** 0 −0.71389 Yes Decreasing P star meaning: *** when p ≤ 0.001; ** when 0.001 < p ≤ 0.01; * when 0.01 < p ≤ 0.05; + when 0.05 < p ≤ 0.1; Empty space when 0.1 < p ≤ 1. It is important to remember that, in aerobiology, there is no universally recognized definition of pollen season and the different calculation criteria used to obtain the start and end dates of a season (and consequently its duration) can influence the results [44]. In this work, when we talk about the season or sporulation pollen of a taxon, we are referring to the start and end dates calculated according to Jäger et al. [11], i.e., the most widely used criterion in Italian monitoring stations: pollen (or sporulation) season starts the first day with a count greater than 1% of the Annual Pollen Integral and it ends when 95% of the Annual Pollen Integral is attained.
Sustainability 2023, 15, 6150 9 of 15 Sustainability 2023, 15, x FOR PEER REVIEW 9 of 15 3.2. Pollen Trends in Rome In order to represent the aerobiological data in a homogeneous and comparable way In order to represent the aerobiological data in a homogeneous and comparable way in space and time, as for the other parameters describing air quality, indicators shared and in space and time, as for the other parameters describing air quality, indicators shared and adopted by the entire monitoring network are required. adopted by the entire monitoring network are required. In the activities of information to the public about the results of aerobiological mon- In the activities of information to the public about the results of aerobiological moni- toring, ininthe itoring, the absence absence of of national national or or European European regulatory regulatory references, references, production production indica- indicators, tors, such as Annual Pollen Integral and sporulation integral, are adopted such as Annual Pollen Integral and sporulation integral, are adopted as indicators of the as indicators of the presence in air of allergenic presence in air of allergenic pollen. pollen. AnnualPollen Annual PollenIntegral Integralofof a Taxon a Taxon (APIn) (APIn) is the is the annual annual sumsum of daily of the the daily concentra- concentrations of airborne pollen recorded for a given pollen taxon. The Annual Pollen Integral isisaa tions of airborne pollen recorded for a given pollen taxon. The Annual Pollen Integral parameter that parameter that depends depends on on the the quantity quantityofofairborne airbornepollen pollenofofthethe taxon considered taxon considered in the in monitoring area, on the duration and intensity of the pollen season. the monitoring area, on the duration and intensity of the pollen season. The unit of The unit of measure- ment of the Annual measurement Pollen Integral of the Annual is Pollenis*Pollen Pollen Integral day/m*3.day/m3 . Annual Spore Annual Spore Integral Integral (ASIn) (ASIn) isis the theannual annual sumsumof ofthe thedaily dailyconcentrations concentrations of of the the airbornespores airborne sporesregister registerforforaagiven givenplant plantor orfungal fungaltaxon. taxon. The The Annual Annual Integral Integral is is aa param- param- eterof eter ofwhich whichdepends dependson onthe thequantity quantityof ofairborne airbornespores sporesof ofthe thetaxon taxonconsidered consideredin inthe the monitoring area, on the duration and on the pollen season. The unit monitoring area, on the duration and on the pollen season. The unit of measurement of the of measurement of the integral of annual sporulation is Spore integral of annual sporulation is Spore * day/m [47]. * day/m 3 3 [47]. Generally,the Generally, the simple simple observation observation of of the thevariations variationsofofthe theAnnual Annual Pollen Pollenor or Spore In- Spore tegral [48] Integral [48]does doesnotnotallow allowto toevaluate evaluatewithwith certainty certainty the existence of significant significant variations variations ofthe of theconcentrations concentrationsover overtime time(see (seeFigure Figure5). 5). Figure 5. Cont.
Sustainability 2023, 15, x FOR PEER REVIEW 10 of 15 Sustainability 2023, 15, 6150 10 of 15 Sustainability 2023, 15, x FOR PEER REVIEW 10 of 15 Figure 5. Annual Pollen and Spore Integral in the two aerobiological monitoring stations, RM5 (blue Figure bar) and RM6 Annual 5. (red bar)Pollen and for the Spore2003–2019. period Integral in the two aerobiological monitoring stations, RM5 (blue bar) and RM6 (red bar) for the period 2003–2019. Figure 5. Annual Pollen and Spore Integral in the two aerobiological monitoring stations, RM5 (blue Scientific works on the trend of pollen indicators are generally addressed to the an- bar) and RM6 (red Scientific worksbar)on forthe thetrend periodof2003–2019. pollen indicators are generally addressed to the antici- ticipation or postponement of phenological indicators (start or end of the pollen season) pation or postponement of phenological indicators (start or end of the pollen season) [49,50]. [49,50]. However, Scientific production works on indicators the trend are just as important for evaluating the effects the of an- However, production indicators areofjust pollen indicators as important forare generally evaluating addressed the effects oftoairborne airborne allergenic ticipation pollens pollens or postponement on human health. In this sense the evaluation of the seasonal allergenic on humanof phenological health. In this senseindicators (start or end the evaluation of the ofseasonal the pollen or season) annual or annual integrals, [49,50]. However, representing production these as average values, does not represent the best tool of integrals, representing these asindicators average values, are justdoes as important not represent for evaluating the best tool theforeffects under- for understanding airborne allergenic the impact on the respiration of In atopic subjects. As for pollutants of standing the impactpollens on the on human respiration health. of atopic this sense subjects. thefor As evaluation pollutants of of theanthropic seasonal anthropic or annualorigin, for a more accurate evaluation of the values, temporal variations of the concen- origin, for integrals, a more accurate representing evaluation these of asthe average temporal variations does notofrepresent the best tool the concentrations it trations it seems for understanding useful to rely on the concentrations with the shorter available formediation seems useful to relythe onimpact on the respiration the concentrations with the of atopic shortersubjects. available Asmediationpollutants period, of period, whichwhich anthropic is currently, origin, is currently, for for forapollen morepollen andand accuratespores, spores, evaluation the of the daily dailytheaverage average temporal concentration. variations of the concen- concentration. If treated trations it with If treated seems adequate with useful toaggregation adequate relyaggregation criteria, on the concentrations pollen criteria, dailydaily with pollen concentration the shorter data data available concentration can be mediation can be processed processed like period, which air quality like air data, quality data, is currently, calculating forcalculating pollen andthethe Temporal Temporal spores, trends the dailytrends of the main of the main average allergenic pol- allergenic pollen concentration. len sampled sampled in inRome, If treated Rome,with using using the theSeasonal adequate Seasonal aggregation Kendall Kendall test. test. pollen daily concentration data can be criteria, For the processed period For thelike periodfrom 2003–2019 from 2003–2019 air quality we considered we considered data, calculating 77pollen the Temporal pollentrendsfamilies families andmain and of the theAlternaria the Alternariaspore allergenic pol- sporeand, and, in in this this period, period, the the analysis analysis of len sampled in Rome, using the Seasonal Kendall test. of concentration concentration trends trends showed showed a a slight slight but but statisti- statistically sig- callynificant significant increase increase of of Betulaceae Betulaceae in the inRM6the RM6 station station (0.01 For the period from 2003–2019 we considered 7 pollen families and the Alternaria < (0.01 p ≤ < p 0.05),≤ 0.05), a a statistically statistically significant significant decrease spore and, decrease in inboth thisin both stations stations period, for for Asteraceae theAsteraceae analysis ≤ 0.001 (p ≤for of(pconcentration 0.001 the for the RM5 trends RM5 station, station, showed 0.001 a slight < p0.001 but < for ≤ 0.01 statisti- p ≤ 0.01 the callyfor RM6 the RM6 station) and significant station) increase and Cupressaceae/Taxaceae Cupressaceae/Taxaceae of Betulaceae in the(0.01 (0.01 < p ≤ 0.05(0.01 RM6< station p ≤ 0.05 for the< pRM5for the RM5 station, ≤ 0.05), sta- p ≤ 0.001 a statistically tion,for p ≤the0.001 significant RM6 for the RM6 station); decrease in station); a statistically both stationsa statistically significant for Asteraceaesignificant decrease decrease (p ≤of0.001 Corylaceae for theof Corylaceae (0.01 p ≤ (0.01 RM5
Sustainability Sustainability 2023, 2023, 15, 6150 15, x FOR PEER REVIEW 11 of 15 11 of 15 Figure 6. Cont.
Sustainability Sustainability 2023, 2023, 15, 6150 15, x FOR PEER REVIEW 12 of 15 12 of 15 Figure 6. Kendall Figure trendtrend 6. Kendall test results for allergenic test results pollen for allergenic and Alternaria pollen in theintwo and Alternaria the aerobiological two aerobiological monitoring stations, RM5 (on the left) and RM6 (on the right) for the period 2003–2019. monitoring stations, RM5 (on the left) and RM6 (on the right) for the period 2003–2019. 4. Conclusions 4. Conclusions Pollen Pollen grains grains and spores and spores are part are part of the ofairborne the airborne particulate particulate matter matter and theandaerobio- the aerobio- logical logical monitoring monitoring networks, networks, in sense, in this this sense, are peculiar are peculiar speciation speciation networks networks for particulate for particulate mattermatter and, and, as forasanthropogenic for anthropogenic pollutants, pollutants, it is important it is important to evaluate to evaluate the temporal the temporal vari-vari- ations of the concentrations with a short mediation period. The choice to process an inad- an ations of the concentrations with a short mediation period. The choice to process equateinadequate parameter parameter can, can, in fact, in fact, hide hide the of the existence existence of a statistically a statistically significant significant trend whichtrend which does exist. does exist. In article In this this article seriesseries of daily of daily concentration concentration fromfrom 20032003 to 2019 to 2019 of eight of eight allergenic allergenic taxa taxa (seven(seven botanical botanical families families andandthe the Alternaria Alternaria spore) spore) were were analyzed analyzed with with a asignificant significantim- impor- tance for human portance for human health. health. For considered For the the considered period, period, the the allergenic allergenic taxon taxon presenting presenting thethe highest highest averagecon- average concen- tration in the air in the study area was Cupressaceae/Taxaceae, centration in the air in the study area was Cupressaceae/Taxaceae, followed by Urticaceae followed by Urticaceae and Poaceae. and Poaceae. From the statistical analysis, carried out using the Kendall test corrected for seasonality, From the statistical analysis, carried out using the Kendall test corrected for season- it emerged that, in most cases, the two stations present in the examined area show a ality, it emerged that, in most cases, the two stations present in the examined area show a consistent trend. This result indicates that the observed trend is not due to local phenomena consistent trend. This result indicates that the observed trend is not due to local phenom- but to a general trend of the examined territory. The elaborations carried out have also ena but to a general trend of the examined territory. The elaborations carried out have also highlighted that the flowering calendar influence the concentration levels of the families highlighted that the flowering calendar influence the concentration levels of the families considered over the years [51]. considered over the years. [51]. In particular, significant decreasing trends, in both stations, were observed for Aster- In particular, significant decreasing trends, in both stations, were observed for Aster- aceae, Cupressaceae/Taxaceae and the Alternaria spore. A significant decreasing trend for aceae, Cupressaceae/Taxaceae and the Alternaria spore. A significant decreasing trend for Corylaceae and Oleaceae was observed in the RM6 station and only a significant increasing Corylaceae and Oleaceae was observed in the RM6 station and only a significant increas- trend, for Betulaceae, still in the RM6 station. ing trend,These for Betulaceae, results are still in the offered RM6 station. tools for a more complete assessment of air as supplementary These results quality and itsare offered effects as supplementary on human health in antoolsurbanfor a more complete assessment of environment. air qualityThe andbiological its effectsparticulate, on human health in an urban environment. indeed, contributes to the mass concentration of PM10 The itbiological and is useful particulate, to estimate indeed, contributes daily pollen to the mass concentration concentration as for of PMabiological the other natural 10 and it is useful to estimate daily pollen concentration as for the other natural contributions. The combined assessment of the biological and abiological component abiological con- of tributions. The combined assessment of the biological and abiological atmospheric pollution can make a useful contribution to improving the knowledge component of at-of air mospheric qualitypollution can makeofahuman for the protection useful health. contribution to improving the knowledge of air quality for the protection of human health. Supplementary Materials: The following supporting information can be downloaded at: https: Supplementary Materials: The following supportingChapter //www.mdpi.com/article/10.3390/su15076150/s1. information can bepollen S1: Allergenic downloaded and sporeat: taxa in www.mdpi.com/xxx/s1. this study; Table S1:Chapter PearsonS1: Allergenic correlation pollen and coefficient forspore pollentaxa andinAlternaria this study;in Table RomeS1: Pear- (2003–2019).; son correlation Figure S1: coefficient for pollenplot Pearson correlation andfor Alternaria in Rome pollen and (2003–2019).; Alternaria in Rome Figure S1: Pearson corre- (2003–2019). lation plot for pollen and Alternaria in Rome (2003–2019). Author Contributions: Conceptualization, A.D.M.d.B., R.G., M.A.B. and A.T.; data curation, A.D.M.d.B., Author Contributions: R.G., M.A.B. and A.T.; Conceptualization, A.D.M.d.B., formal analysis A.D.M.d.B., R.G., R.G., M.A.B. M.A.B. and and A.T.; A.T.; data curation, investigation, A.D.M.d.B., A.D.M.d.B., R.G., M.A.B., D.D.F., A.M. and A.T.; methodology, A.D.M.d.B., R.G., M.A.B. andinvestigation, R.G., M.A.B. and A.T.; formal analysis A.D.M.d.B., R.G., M.A.B. and A.T.; A.T.; supervision: A.D.M.d.B., R.G.,validation, A.D.M.d.B.; M.A.B., D.D.F., A.M. A.T.; A.D.M.d.B., and A.T.; methodology, visualization: A.D.M.d.B., A.D.M.d.B., R.G., M.A.B. R.G., M.A.B., D.D.F., and A.M.A.T.; and A.T.; supervision: A.D.M.d.B.; validation, A.D.M.d.B., A.T.; visualization: A.D.M.d.B., R.G., M.A.B., writing—original draft preparation A.D.M.d.B., R.G., M.A.B. and A.T.; writing—review and editing, D.D.F., A.M. and A.T.; writing—original draft preparation A.D.M.d.B., R.G., M.A.B. and A.T.; writ- A.D.M.d.B., A.T.; visualization: A.D.M.d.B., R.G., M.A.B., D.D.F., A.M. and A.T. All authors have read ing—review and editing, A.D.M.d.B., A.T.; visualization: A.D.M.d.B., R.G., M.A.B., D.D.F., A.M. and and agreed to the published version of the manuscript. A.T. All authors have read and agreed to the published version of the manuscript.
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