Association of Allergic Sensitivity and Pollination in Allergic Respiratory Disease: The Role of Pollution

Figures & data

Figure 1 The interaction of pollutants such as PM_2.5 and O₃ with pollen induces: (A) an increase in the production of pollen concentrations, (B) a fragile pollen membrane, and (C) post-translational modifications in the allergenic protein. In all cases, there are increased levels of allergen proteins, which can be processed by antigen-presenting cells, resulting in a type I hypersensitivity inflammation (mechanism mediated by IL-4, IL-5, and IL-13, and an increase in immunoglobulin E), whose main objective is the degranulation of preformed mediators (histamine or tryptase) contained in mast cells, which promotes mucus secretion by goblet cells and bronchospasm, main symptom of asthma.

Abbreviations: PM_2.5, particulate matter of 2.5 micrometers or less; O₃, ozone; IL, interleukin.

Figure 2 Distribution of allergy sensitivity. (A) Venn diagram of patients sensitive to only one allergen (monosensitive) and patients sensitive to two or more (polysensitive), (B) Venn diagram of patients sensitive to indoor allergens and/or pollen, (C) Venn diagram of patients sensitive to and/or different of pollen (trees and/or grasses and/ or weeds).

Figure 3 The main sensitization to aeroallergens in skin prick test.

Figure 4 Allergic sensitivity by disease.

Notes: *p<0.001; †p<0.01; ‡p<0.05. Patients were more sensitive to HDM than to pollens. Both groups were more sensitive to trees than grasses (p<0.001). Likewise, Fraxinus sp. and Cupressaceae family allergens were twice more prevalent than other tree allergens (p<0.05).

Abbreviations: AR, allergic rhinitis; ARwA, allergic rhinitis with asthma; HDM, house dust mite. OR, odds ratio.

Table 1 Seasons Comparison

Variable	C1			C2			C3
	Season 1	Season 2	p	Season 1	Season 3	p	Season 1	Season 4	p
Fraxinus sp.	1161.50 (428–2372.25)	930.5 (292–1384.75)	0.06	1161.50 (428–2372.25)	634 (269–1095)	0.01	1161.50 (428–2372.25)	459 (377.75–644.75)	0.001
Alnus sp.	497 (238.5–1294)	342.5 (148.75–809.25)	0.1	497 (238.5–1294)	56 (8–633)	0.001	497 (238.5–1294)	58 (0–510.5)	<0.001
Cupressaceae	971.5 (489–1371.75)	585.50 (403.75–799.5)	0.01	971.5 (489–1371.75)	525 (359–864)	0.009	971.5 (489–1371.75)	368 (159.25–470)	<0.001
Quercus sp.	6.50 (0–34)	15 (0–36.25)	0.43	6.50 (0–34)	5 (0–50)	0.77	6.50 (0–34)	6 (1.25–22.75)	0.59
TMP	15.67 (14.20–16.78)	16.51 (14.93–19.58)	0.13	15.67 (14.20–16.78)	16.34 (15.22–19.21)	0.071	15.67 (14.20–16.78)	17.09 (14.02–18.22)	0.23
WSP	1.90 (1.61–2.11)	1.86 (1.67–2.11)	0.89	1.90 (1.61–2.11)	1.90 (1.74–2.08)	0.81	1.90 (1.61–2.11)	1.93 (1.70–2.22)	0.53
RH	50.26 (43.77–55.77)	43.55 (34.08–52.95)	0.037	50.26 (43.77–55.77)	59.65 (49.39–69.59)	0.001	50.26 (43.77–55.77)	43.69 (41.26–49.49)	0.02
PM10	57.57 (44.50–66.16)	66.71 (53.54–76.64)	0.04	57.57 (44.50–66.16)	56.95 (48.33–67.52)	0.66	57.57 (44.50–66.16)	53.21 (46.33–60.15)	0.39
PM2.5	27.85 (22.48–29.71)	33 (27.75–38.35)	0.009	27.85 (22.48–29.71)	26.80 (22.20–31.31)	0.85	27.85 (22.48–29.71)	26.27 (22.59–29.31)	0.54
CO	0.96 (0.89–1.09)	0.92 (0.85–1.07)	0.6	0.96 (0.89–1.09)	0.65 (0.52–0.91)	<0.001	0.96 (0.89–1.09)	0.54 (0.46–0.64)	<0.001
NO	36.21 (30.28–40.02)	31.96 (24.14–41.83)	0.37	36.21 (30.28–40.02)	25.26 (17.31–32.04)	<0.001	36.21 (30.28–40.02)	24.72 (22.29–31.89)	0.001
NO2	34.99 (31.84–38.41)	37.36 (33.81–41.89)	0.04	34.99 (31.84–38.41)	32.28 (28.73–34.98)	0.04	34.99 (31.84–38.41)	33.91 (29.28–37.65)	0.39
NOX	70.47 (62.70–77.71)	68.34 (60.32–83.82)	0.98	70.47 (62.70–77.71)	57.76 (45.98–68.97)	0.001	70.47 (62.70–77.71)	58.64 (53.83–70.83)	0.007
O3	20.11 (16.55–26.26)	23.49 (19.05–36.41)	0.02	20.11 (16.55–26.26)	27.76 (18.69–32.82)	0.006	20.11 (16.55–26.26)	23.63 (20–29.35)	0.02
PMCO	30.77 (19.60–32.63)	32.75 (26.63–38.25)	0.1	30.77 (19.60–32.63)	29.90 (24.06–36.78)	0.67	30.77 (19.60–32.63)	27.87 (23.76–31.82)	0.33
SO2	8.22 (5.55–10.16)	7.79 (5.31–17.49)	0.69	8.22 (5.55–10.16)	6.95 (4.43–8.53)	0.63	8.22 (5.55–10.16)	9.69 (6.83–13.57)	0.18
Variable	C4			C5			C6
	Season 2	Season 3	p	Season 2	Season 4	p	Season 3	Season 4	p
Fraxinus sp.	930.5 (292–1384.75)	634 (269–1095)	0.25	930.5 (292–1384.75)	459 (377.75–644.75)	0.021	634 (269–1095)	459 (377.75–644.75)	0.13
Alnus sp.	342.5 (148.75–809.25)	56 (8–633)	0.001	342.5 (148.75–809.25)	58 (0–510.5)	0.001	56 (8–633)	58 (0–510.5)	0.01
Cupressaceae	585.50 (403.75–799.5)	525 (359–864)	0.83	585.50 (403.75–799.5)	368 (159.25–470)	<0.001	525 (359–864)	368 (159.25–470)	<0.001
Quercus sp.	15 (0–36.25)	5 (0–50)	0.82	15 (0–36.25)	6 (1.25–22.75)	0.74	5 (0–50)	6 (1.25–22.75)	0.65
TMP	16.51 (14.93–19.58)	16.34 (15.22–19.21)	0.92	16.51 (14.93–19.58)	17.09 (14.02–18.22)	0.84	16.34 (15.22–19.21)	17.09 (14.02–18.22)	0.65
WSP	1.86 (1.67–2.11)	1.90 (1.74–2.08)	0.67	1.86 (1.67–2.11)	1.93 (1.70–2.22)	0.35	1.90 (1.74–2.08)	1.93 (1.70–2.22)	0.64
RH	43.55 (34.08–52.95)	59.65 (49.39–69.59)	<0.001	43.55 (34.08–52.95)	43.69 (41.26–49.49)	0.59	59.65 (49.39–69.59)	43.69 (41.26–49.49)	<0.001
PM10	66.71 (53.54–76.64)	56.95 (48.33–67.52)	0.022	66.71 (53.54–76.64)	53.21 (46.33–60.15)	<0.001	56.95 (48.33–67.52)	53.21 (46.33–60.15)	0.13
PM2.5	33 (27.75–38.35)	26.80 (22.20–31.31)	0.002	33 (27.75–38.35)	26.27 (22.59–29.31)	<0.001	26.80 (22.20–31.31)	26.27 (22.59–29.31)	0.64
CO	0.92 (0.85–1.07)	0.65 (0.52–0.91)	<0.001	0.92 (0.85–1.07)	0.54 (0.46–0.64)	<0.001	0.65 (0.52–0.91)	0.54 (0.46–0.64)	0.004
NO	31.96 (24.14–41.83)	25.26 (17.31–32.04)	0.003	31.96 (24.14–41.83)	24.72 (22.29–31.89)	0.01	25.26 (17.31–32.04)	24.72 (22.29–31.89)	0.46
NO2	37.36 (33.81–41.89)	32.28 (28.73–34.98)	<0.001	37.36 (33.81–41.89)	33.91 (29.28–37.65)	0.01	32.28 (28.73–34.98)	33.91 (29.28–37.65)	0.23
NOX	68.34 (60.32–83.82)	57.76 (45.98–68.97)	0.001	68.34 (60.32–83.82)	58.64 (53.83–70.83)	0.006	57.76 (45.98–68.97)	58.64 (53.83–70.83)	0.31
O3	23.49 (19.05–36.41)	27.76 (18.69–32.82)	0.54	23.49 (19.05–36.41)	23.63 (20–29.35)	0.8	27.76 (18.69–32.82)	23.63 (20–29.35)	0.18
PMCO	32.75 (26.63–38.25)	29.90 (24.06–36.78)	0.21	32.75 (26.63–38.25)	27.87 (23.76–31.82)	0.003	29.90 (24.06–36.78)	27.87 (23.76–31.82)	0.12
SO2	7.79 (5.31–17.49)	6.95 (4.43–8.53)	0.08	7.79 (5.31–17.49)	9.69 (6.83–13.57)	0.76	6.95 (4.43–8.53)	9.69 (6.83–13.57)	0.003

Abbreviations: TMP, temperature; WSP, wind speed; RH, relative humidity; PM₁₀, particulate matter of 10 micrometers or less; PM_2.5, particulate matter of 2.5 micrometers or less; CO, carbon monoxide; NO, nitrogen monoxide; NO₂, nitrogen dioxide; NO_X, nitrogen oxides; O₃, ozone; PM_CO, coarse fraction of PM₁₀ and PM_2.5 particles; SO₂, sulfur dioxide; C1, comparison 1 (2014–2015 vs 2015–2016); C2, comparison 2 (2014–2015 vs 2016–2017); C3, comparison 3 (2014–2015 vs 2017–2018); C4, comparison 4 (2015–2016 vs 2016–2017); C5, comparison 5 (2015–2016 vs 2017–2018); C6, comparison 6 (2016–2017 vs 2017–2018).

Figure 5 Pollen monitoring (2014–2018). (A) Pollen frequency, (B) Pollen count measured in annual pollen Integral (APIn), (C) Pollen counts by pollination season.

Abbreviations: S1, season 1; S2, season 2; S3, season 3; S4, season 4.

Figure 6 Allergic sensitivity per period by disease.

Notes: *p<0.001; †p<0.01; ‡p<0.05. In the second period (2015–2018), pollen sensitization increased significantly, twice in AR and four times in ARwA (p<0.01). Quercus sp. and Alnus sp. allergens sensitization raised in the AR group (p<0.05), whereas the ARwA group increased sensitization frequencies for Quercus sp., Cupressaceae family, and Alnus sp. (p<0.001). However, Fraxinus sp. sensitization was the one that increased the most in both groups (p<0.001).

Abbreviations: AR, allergic rhinitis; ARwA, allergic rhinitis with asthma; HDM, house dust mite; NS, non-significative; NA, not applicable.

Table 2 Meteorological and Pollutants Analysis Between Pollination and No Pollination Seasons

Variables	Season 1			Season 2			Season 3			Season 4
	Pollination Season	No Pollination Season	p	Pollination Season	No Pollination Season	p	Pollination Season	No Pollination Season	p	Pollination Season	No Pollination Season	p
Fraxinus sp.	1161.5 (428–2372.25)	8.50 (1–24.75)	<0.001	930.5 (292–1384)	37 (9.5–37)	<0.001	634 (269–1095)	22 (7.5–44.75)	<0.001	459 (377.75–644.75)	4.5 (2.75–9)	<0.001
Alnus sp.	497 (238.5–1294)	0.000 (0–1)	<0.001	342.5 (148.75–809.25)	18 (1.5–18)	<0.001	56 (8–633)	4 (2–13.5)	<0.001	58 (0–510.5)	0 (0–0)	<0.001
Cupressaceae	971.50 (489–1371.75)	30.50 (22–69.5)	<0.001	585.5 (403.75–799.5)	196 (37.5–196)	<0.001	525 (359–864)	95 (55.75–212)	<0.001	368 (159.25–470)	214.5 (151–366.25)	0.14
Quercus sp.	6.50 (0–34)	0 (0–0)	<0.001	15 (0.0–36.25)	0.0 (0.0–0.0)	<0.001	5 (0.0–50)	0.0 (0.0–0.0)	<0.001	6 (1.25–22.75)	0 (0–0)	<0.001
TMP	15.67 (14.20–16.78)	17.16 (16.31–17.98)	0.003	16.51 (14.93–19.58)	17.8 (17.01–18.31)	0.042	16.34 (15.22–19.21)	17.46 (17.3–18.07)	0.104	17.09 (14.02–18.22)	17.20 (16.60–18.83)	0.24
WSP	1.90 (1.61–2.11)	2.06 (1.83–2.20)	0.095	1.86 (1.67–2.11)	2.02 (1.80–2.28)	0.067	1.90 (1.74–2.08)	2.11 (1.90–2.45)	0.012	1.93 (1.70–2.22)	2.06 (1.91–2.4)	0.09
RH	50.26 (43.77–55.77)	63.83 (59.99–67.05)	<0.001	43.55 (34.08–52.95)	58.83 (55.75–61.96)	<0.001	59.65 (49.39–69.59)	61.25 (57.85–63.45)	0.54	43.69 (41.26–49.49)	61.98 (56.72–68.24)	<0.001
PM10	57.57 (44.50–66.16)	38.57 (38.80–42.64)	<0.001	66.71 (53.64–76.64)	47.92 (44.32–50.92)	<0.001	56.95 (48.33–67.52)	41 (37.41–46.14)	<0.001	53.21 (46.33–60.15)	37.59 (29.46–42.8)	<0.001
PM2.5	27.85 (22.48–29.71)	18.16 (17.35–22.21)	0.001	33 (27.75–38.35)	26.57 (23.87–29.89)	0.001	26.8 (22.2–31.31)	20.71 (16.4–21.83)	<0.001	26.27 (22.59–29.31)	19.16 (13.8–23.06)	0.002
CO	0.96 (0.89–1.09)	0.87 (0.77–0.93)	0.004	0.92 (0.85–1.07)	0.81 (0.73–0.91)	0.001	0.65 (0.52–0.91)	0.73 (0.65–0.82)	0.128	0.54 (0.46–0.64)	0.54 (0.48–0.68)	0.71
NO	36.21 (30.28–40.02)	23.64 (21.41–29.57)	<0.001	31.96 (24.14–41.83)	23.62 (20.05–28.66)	0.001	25.26 (17.31–32.04)	20.19 (19.10–22.75)	0.078	24.72 (22.29–31.89)	17.58 (15.41–21.55)	0.005
NO2	34.99 (31.84–38.41)	26.68 (24.66–29.74)	<0.001	37.36 (33.81–41.89)	29.85 (27.90–33.91)	<0.001	32.28 (28.73–34.98)	26.96 (24.6–29.82)	0.001	33.91 (29.28–37.65)	30.33 (28.07–31.79)	0.06
NOX	70.47 (62.70–77.61)	51.95 (47.23–57.33)	<0.001	68.34 (60.32–83.82)	55.41 (48.51–59.96)	<0.001	57.76 (45.98–68.97)	49.27 (44.35–53.04)	0.006	58.64 (53.83–70.83)	46.89 (45.77–57.09)	0.007
O3	20.11 (16.55–26.26)	20.44 (17.17–25.42)	0.905	23.49 (19.05–36.41)	26.42 (22.03–27.83)	0.773	27.76 (18.69–32.82)	25.02 (20.32–28.22)	0.327	23.63 (20–29.35)	21.13 (16.82–24.31)	0.04
PMCO	30.77 (19.60–32.63)	17.76 (15.52–21.08)	0.001	32.75 (26.63–38.25)	20.70 (18.61–23.73)	<0.001	29.90 (24.06–36.78)	22.18 (18.25–23.81)	<0.001	27.87 (23.76–31.82)	17.73 (13.67–19.67)	<0.001
SO2	8.22 (5.55–10.16)	4.74 (4.20–5.90)	0.002	7.79 (5.31–17.49)	5.89 (5.01–7.49)	0.027	6.95 (4.43–8.53)	5.21 (4.39–7.06)	0.163	9.69 (6.83–13.57)	5.84 (5.15–7.13)	0.001

Abbreviations: TMP, temperature; WSP, wind speed; RH, relative humidity; PM₁₀, particulate matter of 10 micrometers or less; PM_2.5, particulate matter of 2.5 micrometers or less; CO, carbon monoxide; NO, nitrogen monoxide; NO₂, nitrogen dioxide; NO_X, nitrogen oxides; O₃, ozone; PM_CO, coarse fraction of PM₁₀ and PM_2.5 particles; SO₂, sulfur dioxide; Season 1 (2014–2015); Season 2 (2015–2016); Season 3 (2016–2017); Season 4 (2017–2018).

Table 3 Global Correlations Between Meteorological Variables and Pollution with Pollen

Variables	Fraxinus sp.		Cupressaceae		Alnus sp.		Quercus sp.
	Pearson r	p	Pearson r	p	Pearson r	p	Pearson r	p
TMP	−0.31	<0.001	−0.13	0.16	−0.11	0.24	0.11	0.24
WSP	−0.14	0.11	−0.18	0.03	−0.14	0.12	−0.15	0.1
RH	−0.05	0.56	0.05	0.59	−0.06	0.52	0.03	0.75
PM10	0.50	<0.001	0.44	<0.001	0.31	0.001	0.14	0.12
PM2.5	0.34	<0.001	0.38	<0.001	0.34	<0.001	0.21	0.02
CO	0.37	<0.001	0.38	<0.001	0.25	0.006	0.25	0.01
NO	0.35	<0.001	0.26	0.004	0.29	0.001	0.20	0.03
NO2	0.34	<0.001	0.24	0.008	0.18	0.05	0.15	0.11
NOX	0.37	<0.001	0.27	0.003	0.27	0.003	0.20	0.03
O3	−0.18	0.06	−0.03	0.78	−0.07	0.45	0.03	0.76
PMCO	0.56	<0.001	0.41	<0.001	0.23	0.01	0.07	0.48
SO2	0.14	0.13	0.003	0.97	0.01	0.88	0.17	0.05

Abbreviations: TMP, temperature; WSP, wind speed; RH, relative humidity; PM₁₀, particulate matter of 10 micrometers or less; PM_2.5, particulate matter of 2.5 micrometers or less; CO, carbon monoxide; NO, nitrogen monoxide; NO₂, nitrogen dioxide; NO_X, nitrogen oxides; O₃, ozone; PM_CO, coarse fraction of PM₁₀ and PM_2.5 particles; SO₂, sulfur dioxide.

Figure 7 Seasons correlations between significant meteorological variables and pollutants with pollen.

Notes: The number of significant correlations with pollution variables increased significantly from S1 to S2. The most consistent and significant correlations were found between air pollutants and pollen concentrations in all seasons for PM₁₀, NO₂, and PM_CO with Fraxinus sp. (p<0.02).

Abbreviations: PM₁₀, particulate matter of 10 micrometers or less; NO₂, nitrogen dioxide; PM_CO, coarse fraction of PM₁₀ and PM_2.5 particles; SO₂, sulfur dioxide; Season 1 (2014–2015); Season 2 (2015–2016); Season 3 (2016–2017); Season 4 (2017–2018).