Environment International 78 (2015) 5160

Contents lists available at ScienceDirect

Environment International
journal homepage: www.elsevier.com/locate/envint

Exposure to emissions from municipal solid waste incinerators and

miscarriages: A multisite study of the MONITER Project
S. Candela a,b, L. Bonvicini a,b,, A. Ranzi c, F. Baldacchini a,b, S. Broccoli a,b, M. Cordioli c, E. Carretta a,b,1,
F. Luberto a,b, P. Angelini d, A. Evangelista a,b,2, P. Marzaroli a,b,3, P. Giorgi Rossi a,b, F. Forastiere e
a

Epidemiology Unit, Azienda Unit Sanitaria Locale, Reggio Emilia, Italy

IRCCS Arcispedale Santa Maria Nuova, Reggio Emilia, Italy
Regional Reference Centre on Environment and Health, ARPA Emilia-Romagna Region, Modena, Italy
d
Public Health Service, Emilia-Romagna Region, Italy
e
Department of Epidemiology, Lazio Region, Italy
b
c

a r t i c l e

i n f o

Article history:
Received 21 August 2014
Received in revised form 23 December 2014
Accepted 23 December 2014
Available online 10 March 2015
Keywords:
Miscarriage
Spontaneous abortion
Incinerator exposure
Abortion risk factors

a b s t r a c t
Background: Miscarriages are an important indicator of reproductive health but only few studies have analyzed
their association with exposure to emissions from municipal solid waste incinerators.
This study analyzed the occurrence of miscarriages in women aged 1549 years residing near seven incinerators
of the Emilia-Romagna Region (Northern Italy) in the period 20022006.
Methods: We considered all pregnancies occurring in women residing during the rst trimester of pregnancy
within a 4 km radius of each incinerator. Addresses were geocoded and exposures were characterized by a dispersion model (ADMS Urban model) producing pollution maps for incinerators based on PM10 stack measurements and for other pollution sources based on NOx ground measurements. Information on pregnancies and
their outcomes was obtained from the Hospital Discharge Database. Simplied True Abortion Risks
(STAR) 100 estimated pregnancies were calculated. We ran logistic regressions adjusting for maternal characteristics, exposure to other sources of pollution, and sites, considering the whole population and stratifying by
miscarriage history.
Results: The study analyzed 11,875 pregnancies with 1375 miscarriages. After adjusting for confounders, an increase of PM10 due to incinerator emissions was associated with an increased risk of miscarriage (test for
trend, p = 0.042). The odds ratio for the highest quartile of exposed versus not exposed women was 1.29, 95%
CI 0.971.72. The effect was present only for women without previous miscarriages (highest quartile of exposed
versus not exposed women 1.44, 95% CI 1.061.96; test for trend, p = 0.009).
Conclusion: Exposure to incinerator emissions is associated with an increased risk of miscarriage. This result
should be interpreted with those of a previous study on reproductive health conducted in the same area that observed an association between incinerator exposure and preterm births.
2015 Elsevier Ltd. All rights reserved.

Abbreviations: ADMS, Atmospheric Dispersion Modelling System; BO, Bologna; CI, condence interval; DI, deprivation index; FE, Ferrara; FO, Forl; IAB, induced abortion; ICD-9-CM,
International Classication of Diseases, Ninth Revision, Clinical Modication; IQR, Interquartile Range; I-TEQ, International Toxicity Equivalency Factor; LB, live birth; MO, Modena;
MONITER, Monitoring of incinerators in the Emilia-Romagna territory (MONitoraggio degli Inceneritori nel Territorio dell'Emilia-Romagna); MSWI, municipal solid waste incinerator;
Nm3, normal cubic meter; NOx, nitrogen oxide; OR, odds ratio; PAH, polycyclic aromatic hydrocarbons; PM, particulate matter; RA, Ravenna; RE, Reggio Emilia; RN, Rimini; SAB, spontaneous
abortion; SB, stillbirths; SD, standard deviation; SES, socioeconomic status; STAR, Simplied True Abortion Risks; TEQ, Toxicity Equivalent.
Corresponding author at: Epidemiology Unit, Local Health Authority, Via Amendola 2, 42122 Reggio Emilia, Italy.
E-mail addresses: silvia.candela@gmail.com (S. Candela), laurabonvicini@ausl.re.it (L. Bonvicini), aranzi@arpa.emr.it (A. Ranzi), avia.baldacchini@audl.re.it (F. Baldacchini),
serena.broccoli@ausl.re.it (S. Broccoli), mcordioli@arpa.emr.it (M. Cordioli), elisa.carretta2@unibo.it (E. Carretta), ferdinando.luberto@ausl.re.it (F. Luberto),
pangelini@regione.emilia-romagna.it (P. Angelini), a.evangelist@gmail.com (A. Evangelista), paolo.marzaroli@ausl.bologna.it (P. Marzaroli), paolo.giorgirossi@ausl.re.it (P. Giorgi Rossi),
f.forastiere@deplazio.it (F. Forastiere).
1
Department of Biomedical and Neuromotor Sciences, University of Bologna, Bologna, Italy.
2
Unit of Cancer Epidemiology, San Giovanni Battista Hospital, Turin, Italy.
3
UOC Epidemiologia, Promozione della Salute e Comunicazione del Rischio, Dipartimento di Sanit Pubblica, Azienda Usl di Bologna, Italy.

http://dx.doi.org/10.1016/j.envint.2014.12.008
0160-4120/ 2015 Elsevier Ltd. All rights reserved.

52

S. Candela et al. / Environment International 78 (2015) 5160

1. Introduction
Miscarriage is a pathologic event of pregnancy whose causes are not
entirely clear. Many risk factors, however, have been described, including maternal age (Nybo Andersen et al., 2000), genetic disorders, uterine abnormalities, and hormonal deciency (Garca-Engudanos et al.,
2002). Exposure to several occupational or environmental toxic substances, such as metals, pesticides, solvents, volatile anesthetics, and active or passive tobacco smoke, has also been documented (Kumar,
2011; Pineles et al., 2014; Wigle et al., 2008). As for trafc-related air
pollution, a study performed in California documented a small increased
risk of miscarriage among women living near high-trafc roads (Green
et al., 2009).
No association was found between dioxin exposure and miscarriage in the Seveso study on women followed up to 30 years after
the incident (Wesselink et al., 2014). An increased risk of missed
abortions was detected in a casecontrol study evaluating the effect
of DNA-adducts on polycyclic aromatic hydrocarbons (PAH) in blood
cells but no association was found with PAH levels (Wu et al., 2010)
in abortion tissues.
Three studies have studied the effects of incinerator exposure on
miscarriages. Tango et al. (2004) investigated the association of miscarriages and other adverse reproductive outcomes in women in Japan
living within 10 km of 63 municipal solid waste incinerators with high
dioxin emission levels (above 80 ng international toxic equivalents
TEQ/m3). The study showed no excess of miscarriage or of the other outcomes within 2 km from the incinerator. Vinceti et al. (2008) did not
detect an increased risk of miscarriages in a population of women
aged 1649 years residing or working near the incinerator of Modena,
a northern Italian city in the Emilia-Romagna Region, during the period
20032006. Finally, the project Enhance Health, evaluating the health
status of a population living near the incinerator of Coriano (Forl),
another site in the Emilia-Romagna Region (Enhance Health, 2007) revealed no risk excess of miscarriage in the period 19982003 among
women of childbearing age. In conclusion, recent reviews (Porta et al.,
2009; Wigle et al., 2008) have indicated that the evidence of a relationship between miscarriages or other reproductive outcomes and solid
waste incinerators is inadequate, and that there is thus need for further
research.
A multisite study (the MONITER Project) was conducted in EmiliaRomagna (a region in Northern Italy) on environmental and health
impact of the incinerators operating in the Region. In a previous report,
we analyzed some reproductive events (sex ratio, multiple births, preterm births, small for gestational age) and showed an increased risk of
preterm births in women exposed to incinerator emissions (Candela
et al., 2013). The aim of the present study, performed within the
MONITER Project, was to integrate the previous ndings on reproductive health with the evaluation of occurrence of miscarriage in women
residing near seven incinerators of the Emilia-Romagna Region in the
period 20022006.
2. Methods
2.1. Study design and setting
This study assessed the occurrence of miscarriages in women
aged 1549 who resided during the rst three months of their pregnancy at the same address within a 4 km radius of the seven incinerators in operation in the Emilia-Romagna Region. A 4-km radius was
chosen because beyond that distance it was difcult to assess the
concentration of particulate matter (PM10) attributable to the emissions of the incinerator, while other pollution sources such as trafc,
industries, and domestic heating were more prominent.
All the women who had resided at least one day in any year in the
study period were linked to the Hospital Discharge Database to identify all the subjects who had delivered or had had an abortion

(spontaneous or induced) in the period 20022006. Women who

had resided at the same address in the study area for the rst three
months of pregnancy entered in the study and the pregnancy outcome was analyzed according to the mean exposure to incinerator
emissions during that period. The rst trimester of pregnancy was
identied as the three months after the presumed date of conception, estimated as the day timed 280 days before delivery, in case of
birth, and 90 days before abortion, whether miscarriage or induced
abortion. To line up exposure time for abortions and births at
the two ends of the study period, we included in the analyses all
the pregnancies whose estimated conception date fell between 03
October 2001 and 26 March 2006.
The plants, located in Reggio Emilia, Modena, Bologna, Ferrara,
Ravenna, Rimini, and Forl, are rather different regarding their
starting date (1968 for the Reggio Emilia incinerator, 1999 for Ravenna), technical characteristics, and capacity (from 56,000 t/y for
Ravenna to 180,000 for Bologna), as reported elsewhere (Candela
et al., 2013). The location of the incinerators also differed, ranging
from the immediate outskirts of the cities of Reggio Emilia and
Modena to an industrial district far from residential areas in Ravenna.
These different locations account for the large variability among sites
of population size.
Addresses, dates of birth, and nationalities of all residents were provided by the municipalities and all the addresses were geocoded at
street number using Geographic Information Systems (GIS).

2.2. Exposure
2.2.1. Incinerator exposure
Exposure value due to incinerator emissions was assigned to each
address in the study area by means of dispersion maps of particulate
matter (PM10) using the quasi-Gaussian model Atmospheric Dispersion
Modelling System (ADMS Urban 2.2., Cambridge Environmental Research Consultants, Cambridge, UK), as described elsewhere (Candela
et al., 2013). Since the early 2000s, the law requires that measurements
of particulate matter be collected every 30 min by the monitoring system. During the entire period of our study, more than 17,000 measurements were taken. The very large amount of available data and the good
spatiotemporal correlation with other pollutants emitted from the
incinerators were the two main reasons for choosing PM10 as tracer of
all incinerator pollution, whose measured components are a mix of
heavy metals as dened by the Italian environmental law, including
several metals and metalloids (lead, cadmium, mercury, antimony,
arsenic, chromium, cobalt, copper, manganese, nickel, vanadium, tin),
dioxins/furans, PCB, and PAH (see Appendices A and B) (Biancolini
et al., 2011).
Five yearly simulations were available for each plant for the
period 20022006. For each area, a representative meteorological
year was chosen for the entire period to be used as meteorological
input in the ADMS simulations. A monthly value of exposure to
municipal solid waste incinerator (MSWI) emission was assigned
to each woman based on residence. Each reproductive event was
characterized by the mean exposure during the rst three months
of pregnancy.
The variable was categorized in quartiles on the basis of exposure
values observed throughout the entire period (20022006). Women residing in the study area of Reggio Emilia between January 2003 and June
2005, while incinerator activities were suspended, were considered
non-exposed.
The exposure levels (ng/m3) were thus the following:
level 1: PM10 = 0; level 2: 0 b PM10 0.27; level 3:
0.27 b PM10 0.70; level 4: 0.70 b PM10 1.32; level 5: N1.32.
The maximum exposure level of PM10 was 71.98.

S. Candela et al. / Environment International 78 (2015) 5160

53

Fig. 1. Number of pregnancies in the period 20022006 in the study area.

2.2.2. Exposure to other sources

Pollution maps for exposure to trafc, industry, livestock and
agricultural farms, and heating were developed, using nitrogen
oxides (NOx ) as tracer and ADMS dispersion model to shape the
maps.
Nitrogen oxides were identied as the best tracer of air pollution
derived from other sources, such as trafc, industry, livestock and agricultural farms, and heating. The main reason for this choice was the
completeness of emission data for this pollutant in comparison with
others (particularly for industrial sites).
Information on these pollutants was gathered by up-to-date
documentation.
Exposure (g/m3) to all other sources was categorized in 4 levels according to distribution quartiles:

level 1: NOx b 35.72; level 2: 35.72 b NOx 52.34; level 3:

52.34 b NOx 72.52; level 4: NOx N 72.52.
The maximum exposure level of NOx was 432.55.

2.3. Women's characteristics

Women's age and nationality (Italian or not Italian) were considered in the analysis. Age was calculated on June 30 for each
woman in each year and was categorized in four classes characterized by different miscarriage risks in the general population (Nybo
Andersen et al., 2000): 1520, 2134, 3540, and 4149 years. Socioeconomic condition was assessed through a deprivation index
(DI) dened at census tract level whose distribution was categorized in quintiles. A DI value was assigned to each census track
ranging from 1 (least deprived) to 5 (most deprived) (Caranci
et al., 2010).
For each rst pregnancy during the study period, the Hospital Discharge Database was searched to identify previous miscarriages in the
preceding 4 years.

2.4. Measure of miscarriage

Information on pregnancies and their outcomes was obtained
from the linkage of subjects in study with the Hospital Discharge
Database.
Spontaneous abortion occurrence was studied as the proportion of
all the pregnancies at risk in a given period, estimated by adding all
the live births, the stillbirths, the miscarriages, and a proportion of induced abortions, whose dimension depends on the distribution by gestational age of both induced and spontaneous abortions, since only
those induced abortions that take place later than the time when miscarriages generally occur are considered as pregnancies at risk. This proportion is called Simplied True Abortion Risk (STAR) (Susser, 1983;
Susser and Kline, 1983)
STAR

SAB
 100
SAB LB SB rIAB

where: SAB = spontaneous abortions; LB = live births; SB = stillbirths;

IAB = legally induced abortions; and r = proportion of induced abortions that should be added because at risk of becoming miscarriages,
ranging from 0 to 1. In our study the value of r was set by applying
the procedure proposed by Susser and Kline (1983), calculated by
means of the life-table technique. The analysis is shown in Table C.1
(Appendix C). The value of r thus calculated was 1/2, meaning that
only half of all pregnancies that ended in induced abortions were at
risk of abortion. They were randomly chosen among all the induced
abortions as the gestational age of the event is not provided by the Hospital Discharge Database.
The terms entering into the equation set out above were identied
using the following codes:
Spontaneous abortions: ICD-9-CM codes: 632 and 634 in the principal diagnosis
Induced abortion: ICD-9-CM code: 635 in any diagnoses
Stillbirth: ICD-9-CM codes: V27.1, V27.3, V27.4, V27.6, V23.5, 779.9,
768.0, 768.1, 656.4 in any diagnosis.

54

Table 1
Characteristics of pregnant women and pregnancy outcomes by sites.

a
b
c
d
e

Modena

Ferrara

Ravenna

Rimini

Forl

Bologna

(N = 4351)

(N = 2837)

(N = 220)

(N = 44)

(N = 1380)

(N = 2005)

(N = 1038)

Total
(N = 11,875)

N (%)

N (%)

N (%)

N (%)

N (%)

N (%)

N (%)

N (%)

0.36 (0.75)a
0.14 (0.060.36)a

0.70 (0.93)
0.37 (0.240.84)

0.60 (0.41)
0.50 (0.350.83)

0.84 (0.49)
0.68 (0.451.34)

1.05 (0.45)
0.97 (0.751.23)

1.78 (1.71)
1.18 (0.752.24)

2.78 (3.00)
2.22 (1.383.52)

0.91 (1.51)
0.48 (0.081.14)

61.02 (30.83)
57.54 (39.4280.99)

65.52 (35.03)
59.25 (45.6679.03)

45.66 (33.36)
38.82 (25.4053.08)

17.76 (23.72)
5.35 (5.1027.37)

67.95 (35.42)
60.80 (46.9576.81)

39.32 (20.81)
37.82 (23.4751.59)

40.46 (21.44)
33.83 (26.5050.80)

57.00 (32.33)
52.24 (35.6272.49)

128 (2.9)
3081 (70.8)
981 (22.5)
161 (3.7)
31 (2735)

80 (2.8)
1865 (65.7)
764 (26.9)
128 (4.5)
32 (2836)

11 (5.0)
142 (64.5)
58 (26.4)
9 (4.1)
32 (28.536)

2 (4.5)
32 (72.7)
10 (22.7)
0 (0.0)
31 (27.534)

3200 (73.5)
1151 (26.5)
0 (0.0)

1966 (69.3)
863 (30.4)
8 (0.3)

205 (93.2)
15 (6.8)
0 (0.0)

41 (93.2)
3 (6.8)
0 (0.0)

922 (21.2)
873 (20.1)
911 (20.9)
879 (20.2)
766 (17.6)

576 (20.3)
378 (13.3)
534 (18.8)
487 (17.2)
862 (30.4)

62 (28.2)
39 (17.7)
64 (29.1)
21 (9.5)
34 (15.5)

3543 (95.3)
174 (4.7)

2343 (96.0)
97 (4.0)

3396 (78.1)
17 (0.4)
445 (10.2)
493 (11.3)

2158 (76.1)
19 (0.7)
325 (11.5)
335 (11.8)

28 (2.0)
918 (66.5)
374 (27.1)
60 (4.3)
32 (2935)

42 (2.1)
1330 (66.3)
543 (27.1)
90 (4.5)
32 (2935)

31 (3.0)
632 (60.9)
323 (31.1)
52 (5.0)
33 (2936)

322 (2.7)
8000 (67.4)
3053 (25.7)
500 (4.2)
32 (2835)

1186 (85.9)
194 (14.1)
0 (0.0)

1695 (84.5)
310 (15.5)
0 (0.0)

865 (83.3)
173 (16.7)
0 (0.0)

9158 (77.1)
2709 (22.8)
8 (0.1)

14 (31.8)
26 (59.1)
0 (0.0)
4 (9.1)
0 (0.0)

39 (2.8)
244 (17.7)
591 (42.8)
348 (25.2)
158 (11.4)

726 (36.2)
468 (23.3)
209 (10.4)
321 (16.0)
281 (14.0)

328 (31.6)
272 (26.2)
106 (10.2)
133 (12.8)
199 (19.2)

2667 (22.5)
2300 (19.4)
2415 (20.3)
2193 (18.5)
2300 (19.4)

188 (97.4)
5 (2.6)

37 (97.4)
1 (2.6)

1166 (96.9)
37 (3.1)

1624 (95.6)
75 (4.4)

846 (96.2)
33 (3.8)

9747 (95.9)
422 (4.1)

162 (73.6)
1 (0.5)
28 (12.7)
29 (13.2)

33 (75.0)
0 (0.0)
7 (15.9)
4 (9.1)

1072 (77.7)
2 (0.1)
163 (11.8)
143 (10.4)

1561 (77.9)
10 (0.5)
258 (12.9)
176 (8.8)

767 (73.9)
2 (0.2)
149 (14.4)
120 (11.6)

9149 (77.0)
51 (0.4)
1375 (11.6)
1300 (10.9)

2196 events with no exposure are not considered.

1: less deprived, 5: most deprived.
Only rst events in the study period are considered.
The percentages correspond to STAR: spontaneous abortion / spontaneous abortion + 1/2 induced abortion + births (live births and stillbirths).
Only half induced abortion are considered.

S. Candela et al. / Environment International 78 (2015) 5160

Characteristics
Incinerator exposure
PM10 level ng/m3
Mean (SD)
Median (IQR)
Exposure to other sources
NOx level g/m3
Mean (SD)
Median (IQR)
Maternal age (years)
b=20
2134
3540
4149
Median (IQR)
Nationality
Italian
Foreign
Missing
Deprivation index
SES levelb
1
2
3
4
5
Previous spontaneous abortionc
None
One or more
Pregnancy outcomes
Childbirths (live births)
Childbirths (stillbirths)
Spontaneous abortionsd
Induced abortionse

Reggio Emilia

S. Candela et al. / Environment International 78 (2015) 5160

55

Table 2
Spontaneous abortions (SAB), estimated pregnancies at risk, Simplied true Abortion Risk (STAR), Crude and Adjusted ORs of SAB and 95% CI (SAB = 11,875).
Characteristics
Incinerator exposure levelsb
PM10 level ng/m3
1 (PM10 = 0)
2 (0 b PM10 0.27)
3 (0.27 b PM10 0.70)
4 (0.70 b PM10 1.33)
5 (PM10 N 1.33)
Test for trend p-value
Exposure to other sourcesb
NOx level g/m3
1 (NOx 35.72)
2 (35.72 b NOx 52.34)
3 (52.34 b NOx 72.52)
4 (NOx N 72.52)
Maternal ageb
b=20
2134
3540
4149
Nationalityb
Italian
Foreign
Deprivation indexb
SES levelc
1
2
3
4
5
Site
RE
MO
BO
FE
RA
FO
RN

Estimated pregnancies (n = 11,875)

STAR

Crude OR

95% CI

Adjusted ORa

216
256
277
309
317

2196
2412
2423
2412
2432

9.84
10.61
11.43
12.81
13.03

1 (Ref.)
1.09
1.18
1.35
1.37

(0.901.32)
(0.981.43)
(1.121.62)
(1.141.65)

1 (Ref.)
1.05
1.14
1.29
1.29

355
358
352
307

2991
2969
2949
2956

11.87
12.06
11.94
10.39

1 (Ref.)
1.02
1.01
0.86

(0.871.19)
(0.861.18)
(0.731.01)

1 (Ref.)
1.05
1.05
0.95

(0.891.25)
(0.881.26)
(0.801.14)

23
710
471
171

322
8000
3053
500

7.14
8.88
15.43
34.20

1 (Ref.)
1.27
2.37
6.76

(0.821.95)
(1.533.67)
(4.2510.73)

1 (Ref.)
1.34
2.52
7.18

(0.862.08)
(1.623.94)
(4.4611.55)

1058
313

9158
2709

11.55
11.55

1 (Ref.)
1.00

(0.881.14)

1 (Ref.)
1.17

(1.021.36)

314
262
279
261
259

2667
2300
2415
2193
2300

11.77
11.39
11.55
11.90
11.26

1 (Ref.)
0.96
0.98
1.01
0.95

(0.811.15)
(0.821.16)
(0.851.21)
(0.801.13)

1 (Ref.)
0.99
1.04
1.09
1.00

(0.821.19)
(0.861.25)
(0.911.32)
(0.831.20)

445
325
149
28
7
258
163

4351
2837
1038
220
44
2005
1380

10.23
11.46
14.35
12.73
15.91
12.87
11.81

1 (Ref.)
1.14
1.47
1.28
1.66
1.30
1.18

(0.981.32)
(1.211.80)
(0.851.93)
(0.743.75)
(1.101.53)
(0.971.42)

1 (Ref.)
0.97
1.14
1.15
1.72
1.04
0.93

(0.791.18)
(0.851.53)
(0.721.84)
(0.783.81)
(0.811.33)
(0.711.22)

Spontaneous abortions (n = 1375)

95% CI

(0.851.30)
(0.881.47)
(0.981.70)
(0.971.72)
0.042

Adjusted for exposure to NOx, maternal age, nationality, SES and sites.
Overall OR is a weighted average of the ORs observed in each stratum of the other covariates. The weight of each stratum estimate is proportional to the inverse of the OR variance, i.e.
estimates from small centres have high variance estimates and have smaller inuence on the overall OR estimate than estimates from large centres, which have little variance.
c
1: less deprived, 5: most deprived.
b

Live births: ICD-9-CM codes: 650 and V27 in any diagnosis, if the delivery was not a stillbirth.
2.5. Statistical methods
We performed descriptive analyses of exposure to incinerator
(PM10) and to other sources (NOx), of women's characteristics (age, nationality, deprivation index, length of residence, and previous miscarriages) and of pregnancy outcomes (live birth, stillbirth, miscarriage,
induced abortion) by site.
A multivariate logistic regression model was performed to test the
association between exposure to incinerator emissions, categorized by
quartiles, and miscarriage by means of the Simplied True Abortion
Risk (STAR), adjusting for exposure to other sources, categorized by
quartiles, sites, and maternal covariates: age, nationality, SES. The
odds ratios (ORs) and the relative 95% condence intervals (CI) were
presented and a test for trend across exposure to incinerator emissions
categories was also performed.
A multilevel logistic model, including the same explanatory variables, was performed to test whether the population at each site could
be considered a random sample of one homogeneous population.
We also performed the multivariate logistic regression model including the interaction between incinerator exposure and the history
of spontaneous abortion in the preceding four years. Stratum specic

OR was calculated through linear combination. Only rst pregnancies

in the study period were considered to evaluate possible previous miscarriage. In order to take into account the clustering of observations
within mothers, we estimated all logistic models with robust standard
errors based on the Huber/White/Sandwich estimator (White, 1980)
of variance.
Data analysis was performed using Stata IC 13.
3. Results
During the period 20022006, there was a yearly average of 59,568
women aged 1549 years residing in the study area, with a mean age of
33.9 years (standard deviation: 9.02) and Italian nationality in 83% of all
subjects. There were 15,908 pregnancies beginning in the period from
03 October 2001 to 26 March 2006, but only 13,176 were of women certainly residing at the same address throughout the rst three months of
their gestation. These pregnancies resulted in 9149 live births, 51 stillbirths, 2601 induced abortions, and 1375 miscarriages (Fig. 1). To estimate the total number of pregnancies at risk of abortion, only half of
all the induced abortions, chosen at random, were added to the other
terms in the denominator, so that a total of 11,875 pregnancies were
examined in our study.
Sites were different for all the environmental and sociodemographic characteristics of pregnant women (Table 1). A notable

56

S. Candela et al. / Environment International 78 (2015) 5160

Table 3
Stratied analyses of association between spontaneous abortion (SAB) and incinerator exposure by history of previous abortion. Adjusted ORs and 95% Condence Interval (CI).
Previous spontaneous abortiona interaction p-value =
0.190

Incinerator exposure
PM10 level ng/m3
1
2
3
4
5
p for trend

None (N = 9735)

One or more (N = 419)

ORb

95% CI

ORb

95% CIb

Ref.
1.09
1.26
1.45
1.44
0.009

(0.851.38)
(0.961.66)
(1.081.94)
(1.061.96)

Ref.
0.92
0.57
0.69
0.63
0.211

(0.402.11)
(0.221.47)
(0.281.67)
(0.261.52)

(Only rst events in the study period are considered).

Adjusted for exposure to NOx, maternal age, nationality, SES and sites. Overall OR is a
weighted average of the ORs observed in each stratum of the other covariates. The weight
of each stratum estimate is proportional to the inverse of the OR variance, i.e. estimates
from small centres have high variance estimates and have smaller inuence on the overall
OR estimate than estimates from large centres, which have little variance.
b

difference was seen in the exposure levels to incinerator emissions

(median from 0.14 ng/m 3 [IQR: 0.060.36] for Reggio Emilia to
2.22 ng/m3 [IQR: 1.383.52] for Bologna). The median exposure to
other sources was the highest in Rimini (60.8 g/m3) and the lowest
in Ravenna (5.35 g/m3). Maternal age at birth was lower in Ravenna
and Reggio Emilia (22.7% and 26.2% of mothers N 34 years old, respectively), than in Bologna (36.1%) and between these two extremes in the other sites. The proportion of foreign women was
high in Modena (30.4%) and Reggio Emilia (26.5%), and much
lower in the other sites. In line with this proportion was the socioeconomic status of the women. The proportion of women in the
study with a miscarriage preceding the rst pregnancy considered
was rather similar among sites.
The proportion of spontaneous abortions differed among the sites
(from 10.2 abortions per 100 estimated pregnancies [95% CI 9.311.2
(data not shown in the table)] in Reggio Emilia to 15.9 [6.630.1 (data
not shown in the table)] in Ravenna), while childbirths and stillbirths
were more evenly distributed. The proportion of induced abortions considered in our analysis was somewhat different among sites: from 8.8%
in Forl to 13.2% in Ferrara, while in Reggio Emilia, Modena, and Bologna,
it was rather similar.
Table 2 shows the logistic regression of miscarriages on exposure
levels to incinerator emissions, presenting both crude and adjusted
ORs. There is a positive association between the exposure levels to incinerator emissions and miscarriages, especially considering the third
and fourth levels in the crude analysis. After adjusting for covariates,
the ORs decrease slightly but a trend of increasing risk with increasing
exposure is present (p for trend = 0.042). Neither the exposure to
other sources nor the socioeconomic status, indicated by the deprivation index, was associated with the outcome, while maternal age was
strongly related. Women's nationality and sites show different results
in the crude and in the adjusted analyses. In fact, being a foreign
woman carries a risk of increased miscarriages only after correction
(Crude OR: 1.00 [95% CI 0.881.14]; Adjusted OR: 1.17 [1.021.36]).
Most sites showed a higher risk of miscarriage than the reference (Reggio Emilia) both in the crude analysis and after adjustment, but in the
latter risk decreased until about the unit in almost all sites.
Sites were strongly associated with miscarriages, but there was
no interaction with other determinants and in particular with PM10
due to incinerators. In other words, for the OR estimating the association between exposure and spontaneous abortions, the population

at each site can be considered as a random sample of one homogeneous population (intracluster correlation Rho b 10^ 11, data not
shown).
An analysis similar to that reported in Table 2 was also performed on
data stratied by history of previous spontaneous abortion (only rst
pregnancies in the study period) (Table 3). A positive association between spontaneous abortion and exposure to incinerator emissions
was observed only for women without a history of previous miscarriages (test for trend, p 0.009).
4. Discussion
In this population-based study on the pregnancies occurring during the period 20022006 in the 4 km radius around the 7 incinerators in the Emilia-Romagna Region, we observed a slightly increased
risk of miscarriages with increasing maternal exposure to incinerator
emissions (OR of the two highest exposure levels compared to the
non-exposed: 1.29, 95% CI 0.981.70 and 1.29 95% CI 0.971.72, respectively) (Table 2). The association was observed only for those
pregnancies not preceded by a miscarriage in the previous four
years (Table 3).
Our ndings differ from those of the previous three studies on the
same subject. In the Japanese study (Tango et al., 2004), incinerator
exposure was assessed only by means of distance of individual addresses from the corresponding incinerator. More recent literature
shows that distance is a weak proxy for exposure, which can be
much better determined through a dispersion model (Cordioli
et al., 2013; Ashworth et al., 2013). The two Italian studies
(Enhance Health, 2007; Vinceti et al., 2008) evaluated the occurrence of miscarriages as the rate measured in women of childbearing
age. This measure can obviously be affected by different attitudes towards childbearing in different groups of people, relating to age, culture, income, and religious belief. A proper analysis of this outcome
in a population-based study might consider spontaneous abortions
as the proportion of all pregnancies at risk, determined by means of
the equation proposed by Susser and Kline (1983) and presented in
our Methods section. Moreover, these studies analyzed small populations living near one incinerator plant. Lastly, we examined the
exposure to incinerator emissions during the rst trimester of pregnancy, the period in which the risk of miscarriage is higher. For this
reason, we made sure that only those women certainly residing at
the same address during the rst three months of gestation entered
in the study and each of them was characterized by the exposure to
incinerator emissions during that period.
The maternal characteristics analyzed in our study are major (maternal age) or uncertain (nationality, socioeconomic status) risk factors
of miscarriage. In fact, our study conrms that maternal age is a very
important risk factor (Adjusted OR N 7 for women N 40 years old
when compared to the younger women). Foreign nationality shows
a weak association with spontaneous abortion after adjustment, essentially conrming the results of a Regional Survey on the health
of foreigners (Pacelli et al., 2011). Socioeconomic status does not
seem to affect the outcome, but deprivation index was specially
calculated at census tract level in the site areas where differences
in socioeconomic status were not so large. In any case, there are
only a few studies on this association and their nal results are inconsistent (Osborn et al., 2000; Parazzini et al., 1991). We could
not nd any association between the exposure to other sources of
pollution and miscarriages; the only previous study about the effect
of trafc pollution and miscarriage found a weak, non-signicant association (ref Green et al., 2009). In the study areas, exposure to pollution from other sources tended to be inversely related to
incinerator exposure (Table 2) due to the location of incinerators
on the outskirts of cities.
The difference in outcome frequency among sites (Table 1) could
be partially produced by different treatments of choice, leading to

S. Candela et al. / Environment International 78 (2015) 5160

different hospitalization rates. Since the Hospital Discharge Data

Base is the only available source of information in our study, this
point has been critically evaluated. Hospitalization after a miscarriage depends on the treatment chosen by the woman or prescribed
by the physician in charge to remove any placental tissue or to terminate non-viable pregnancies. Only surgical treatment (vacuum aspiration or uterine dilatation and curettage) takes place in a hospital
setting, even as day surgery, while women on pharmacological therapy (misoprostol) or, even more reasonably, on expectant care are
treated as outpatients and the proportion of hospitalizations may
differ from hospital to hospital, and thus from site to site. In the
study period (20022006), pharmacological treatment was not at
all commonplace in Emilia-Romagna and expectant care was rather
infrequent. We therefore think that differential treatment is
unlikely. Nevertheless, despite the very high prevalence of surgery
management of miscarriages in all the study areas, sites were considered as confounders in our main analyses, thus limiting the effect of
any differential treatment. Nevertheless, we cannot rule out the possibility of a residual confounding due to sites, because a similar distribution of outcome proportion could also be seen in the provinces
to which sites belong, at least in the extreme two: Reggio Emilia
(10.8%) and Bologna (13.4%). In conclusion, the difculty of certainly
identifying all the pregnancies occurring in a population, due to possible different treatment among hospitals, is the main issue of a
population-based multisite study on spontaneous abortions; further
research on the subject is required to improve the quality of data
analyzed.
The exposure assessment was based on maternal residence and
did not include any information either on workplace or on possible
displacement during the rst trimester of pregnancy. However, the
potential variability of individual exposure assessment would lead
to non-differential misclassication and would likely tend to mask
the detected association, leading to results biased towards the null.
While no information on other relevant known risk factors, including smoking (Kumar, 2011; Pineles et al., 2014; Wigle et al., 2008)
or excessive alcohol intake, was available, there was no evidence of
their differential distribution within the study area.
We used a geographical approach to assign exposure to environmental pollution, separating the exposure to incinerators from other
relevant sources in the study areas. This approach was used in previous
studies (Candela et al., 2013; Lin et al., 2006; Ranzi et al., 2011; Viel et al.,
2008) and its usability in environmental epidemiology studies of point
sources is well validated (Cordioli et al., 2013; Ashworth et al., 2013;
Floret et al., 2006).
In our study the exposure effect could be observed only for women
without a history of previous spontaneous abortion (Table 3). For this
analysis we considered only the rst pregnancies during the study period so as to avoid analyzing a miscarriage either as an outcome or as a
stratication variable. Thus, the proportion of pregnancies considered
in each year decreased from the rst year (all pregnancies analyzed)
to the subsequent years, when the probability that a woman had
already experienced a pregnancy during the study period gradually
increased, but this effect was evenly spread throughout all the exposure
levels.
The lack of association between miscarriages and exposure to incinerator emissions in women with a previous miscarriage was not unexpected, since an adverse obstetrical history, suggested by a previous
spontaneous abortion, is a well-known risk factor (Makhlouf et al.,
2014; Rai and Reagan, 2006) and it is possible that the presence of
this stronger determinant hid the effect of a weaker one, like exposure
to incinerator emissions.
Another critical issue when one studies miscarriages is their possible mingling with misclassied induced abortions, with a likely differential recording among hospitals. But in this case one would
expect an inverse relation between the distributions of the two outcomes, which was not observed in our study. In particular, the two

57

sites with the lowest and the highest proportion of miscarriages

(Reggio Emilia: 11.1% and Bologna: 15.2%) show a very similar occurrence of induced abortions (Reggio Emilia: 11.9%, Bologna:
11.7%).
These results can be interpreted with those of the other study
conducted within the MONITER Project on reproductive health,
which highlighted an association between preterm births and incinerator exposure, but not with NOx from other sources, during
almost the same period considered here (Candela et al., 2013). A
similar association between preterm and coke production and
steel making facilities has been observed by a recent study in the
US (Porter et al., 2014). It may be possible that preterm births
and miscarriages share common causal factors implied in the termination of pregnancy (Saraswat et al., 2010). In both studies, particulate matters emitted from the incinerators were considered as
a tracer of the pollution produced by these plants and thus as
the marker of the exposure gradient, regardless of their absolute
quantitative value. The particles emitted by these plants are largely
composed of heavy metals, dioxins and dioxin-like substances,
PAHs, and other organic carbon compounds absorbed in them. In
particular, we found in the substances emitted from the EmiliaRomagna plants very low concentrations of dioxins/furans
(Grosso et al., 2012), PCB and PAH, and relevant concentrations
of heavy metals, which were, however, always below the permissible limits (Biancolini et al, 2011) (see Appendix B). This mix of
different substances is similar to that produced by other combustion processes of organic compounds, though the relative contribution of each pollutant may be different. Mechanisms through which
incinerator pollutants may lead to miscarriage have not yet been identied. However, in accordance with the hypothesized mechanisms of air
pollution on preterm births, inammation, direct toxic effects on fetuses
and placenta, displacement of the oxygen-hemoglobin dissociation
curve, and formation of DNA adducts are the possible effects of environmental air pollution (Shah and Balkhair, 2011).
5. Conclusion
Our study examined a possible association between miscarriages
and the exposure to incinerator emissions throughout pregnancy, a subject on which only a few studies have been published. Our study considered a large population of pregnancies in a multisite study, assessing the
exposure with good precision and measuring the abortion occurrence as
accurately as possible. Our study results raise the suggestion of a slight
effect of incinerator pollution, even at a low level, on this reproductive
event. These results may be interpreted with our previous ndings on
the association between levels of exposure to incinerator emissions
and preterm births.
Acknowledgments
We thank Eleonora Verdini and Stefano Sforza (Regional Health Systems Ofce) for the linkage of women database with Hospital Discharge
database.
Finally, we would like to mention the scientic support received by
teachers and colleagues of the Masters in Epidemiology program of
the University of Turin (Italy).
This study was funded by the Regione Emilia-Romagna, Italy (Del. N
466, 11 April 2007), as a part of the Moniter Project (monitoring Incinerators in the Territory of Emilia-Romagna Region) and by the Italian
Ministry of Health, as a part of the Strategic Project "Impatto sanitario
associato alla residenza in siti inquinati, in territori interessati da
impianti di smaltimento/incenerimento riuti ed alla esposizione a
inquinamento in aree urbane" (Ministero della salute - Ricerca
nalizzata 2006 ex art.12 DLgs 502/1992). The authors declare no conicts of interest.

58

S. Candela et al. / Environment International 78 (2015) 5160

Appendix A

SIMULATIONS OF BOLOGNA AREA

Metals

Annual simulation

September-March
simulation

April-August simulation

PM10 M SWI

Fig. A.1. PM10 and metal simulations in different seasons in Bologna area.

S. Candela et al. / Environment International 78 (2015) 5160

59

Appendix B

the probability that a pregnancy having survived up to the end of interval x, will spontaneously end during the interval x + 1 (Table C.2).

Table B.1
Comparison between observed and permitted values for parameters dened following
sampling methodologies provided by law.

Table C.2
Estimation of the true ratio of spontaneous abortion after Susser and Kline.

Parameter

Unit of
measure

Total particulate
Dioxins and furans

mg/Nmc
pg
I-TE/Nmc
PCB
ng/Nmc
PAH
ng/Nmc
Total metals (group ng/Nmc
1)
Total metals (group ng/Nmc
2)
Mercury
ng/Nmc

Extreme values

Mean
values
observed

Permitted
value*

Maximum Minimum

0.063
0.303

0.154
0.348

0.040
0.268

5
100

0.266
5.550
61.400

0.442
10.530
104.500

0.128
1.420
18.200

10,000
500

0.002

0.003

0.001

50

4.300

7.900

0.600

50

Gestational
interval x
(weeks)

Observed at
termination
N.
SAB

N. IA

b=8
910
1112
N12
Total

2028
1921
844
458
5251

3644
3907
1549
291
9391

pregnancies
(px)

qx = fx /
(px 1 / 2jx)

Adjusted
number of
SAB cx = qx
p ici b x

51,568
45,896
40,068
37,675

0.0408
0.0437
0.0215
0.0122

2102.28
2162.45
1016.04
564.88
5845.65

N
births

36,926

P: total number of pregnancies (51,568).

Px: pregnancies that survive to the beginning of the gestational interval x.
fx: number of spontaneous abortions terminating during the gestational interval x.
jx: number of induced abortions terminating in the gestational interval x.

Total metals (group 1): antimony + arsenic + lead + total chrome + cobalt + copper +
manganese + nickel + vanadium.
Total metals (group 2): cadmium + thallium.
*Corresponding to values dened by law with the exception of total particulate for which
the law denes a limit of 10 mg/Nmg.

From: Biancolini V. LINEA PROGETTUALE 1 Caratterizzazione del

materiale particolato emesso dagli inceneritori in esercizio nelle aree
di indagine. In:I risultati del progetto Moniter. Gli effetti degli
inceneritori sull'ambiente e la salute in Emilia-Romagna. Quaderni di
Moniter 04N11. 2011 p. 29.
Appendix C
To identify the value of r, coefcient of the number of induced
abortion (IA) to insert in the Simplied True Abortion Risk (STAR) equation, we applied the procedure proposed by Susser and Kline1. In this
approach an estimate of the true risk of spontaneous abortion (SAB) is
calculated through the life-table technique and is compared to STAR calculated dening r = 1/2.
The discrepancies between the STAR and the true risk are thus
identied. If the STAR underestimates or overestimates the true rate,
the value of r could be modied accordingly: r = 1/3 or r = 2/32.
We used the distributions of SAB and IA by gestational age of the
year 2006 in Emilia-Romagna Region, obtained from the Hospital Discharge Database (Table C.1).

Table C.1
Hospital discharges following hospitalization for spontaneous abortion and induced abortion by weeks of amenorrhea. Women residing in Emilia Romagna Region, year 2006. Absolute numbers and percentages.
Weeks of amenorrhea
b=8
No.
Spontaneous
abortiona
Induced abortionb
a
b

910
%

No.

N12

1112
%

No.

2028 38.62 1921 36.58

No.

Total

Estimated true risk = 11.3 (5845.65 / 51,568).

STAR (r = 1/2) = 11.2.
By setting r = 1/2, the STAR slightly underestimates the estimated
true risk (difference of 0.1).
However, by dening r = 1/3, the STAR overestimates the true risk
and the discrepancy is larger (0.3) (Table C.3).
Table C.3
Value of the Simplied True abortion Risk (STAR) by different values of r.
r

STAR

1/4
1/3
1/2
2/3

11.8
11.6
11.2
10.8

In these data the best estimation for the risk of spontaneous abortion
is obtained by considering r = 1/2.
References
1. Susser E., Kline J. Effects of induced abortion on spontaneous abortion
rates. In: Hemminki K., Sorsa M., Vainio H., eds Occupational Hazards
and Reproduction. Washington, DC: Hemisphere Publishing Corporation, 1983
2. Susser E. Spontaneous abortion and induced abortion: an adjustment
for the presence of induced abortion when estimating the rate of
spontaneous abortion from cross-sectional study. Am J Epidemiol
1983; 117:30508
3. http://www.istat.it/it/archivio/11072
4. Relazione sull'interruzione volontaria di gravidanza in EmiliaRomagna nel 2006. Alcune tendenze. 2007. Assessorato politiche
per la salute RER.
5. Banca Dati CedAP, http://www.saluter.it

844 16.07 458 8.72 5251

3644 38.80 3907 41.60 1549 16.50 291 3.10 9391

3

Source: ISTAT, data from D11 model database.

Source: Emilia-Romagna Region, data from D12/Istat model database.4

In 2006, the number of births to women residing in Emilia-Romagna

was 36,926 (of which 95 were stillbirths).5
The procedure corrects the number of SAB observed in a given gestational interval in order to estimate the additional number of SAB
that would have occurred in absence of IA. Thus, the method estimates

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