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Better IVF outcomes following improvements in laboratory air quality

  • McGill University research institute

Abstract and Figures

Background: It has been proved that air quality is crucial for the success of IVF because of the presence of volatile organic compounds (VOCs), microbes, and perfumes, all of which can be harmful to embryo development in vitro. Therefore IVF laboratories are equipped with high efficiency particulate air (HEPA), and activated carbon filters plus positive pressure for air particulate control, with or without CODA system. Here we introduce a new technology using specially treated Honeycomb matrix media aligned in the Landson ™ series system for our laboratory air purification and its impact on IVF outcome. Methods: Air samples were collected outside and inside the laboratory, and intra-incubator at three different time points, before and after changing carbon filters and after Landson system installation, and we correlated air compounds measure variation with IVF outcome from 1403 cycles. Results: An improvement of air quality was confirmed with passages of total VOCs from 0.42 mg/m(3), 30.48 mg/m(3), 9.62 mg/m3, to 0.1 mg/m(3), 2.5 mg/m(3), 2.19 mg/m(3) through 0.07 mg/m(3), 0.16 mg/m(3), 0.29 mg/m(3), outside the laboratory, inside laboratory and intra-incubator respectively at three separated air sampling times. A clear decrease was observed in some VOCs such as formaldehyde, ethylene, acethylene, propylene, SO2, pentane, NOx, benzene, Hallon-1211, CFC and alcohol. At the same time a significant difference (P<0.05) was found between the third testing time TT3 after carbon filter change and Landson system installation and the first testing time TT1 before carbon filter change in fertilization rate 83.7 % vs 70.1 %, embryo cleavage rate 97.35 % vs 90.8 %, day 5 blastocyst formation rate 51.1 % vs 41.7 %, and pregnancy/implantation rates 54.6 %, 34.4 % vs 40.6 %, 26.4 %. Conclusion: Air purification by the new technology of Landson ™ series significantly improved IVF laboratory air quality, and embryo quality, thus increased pregnancy and implantation rates.
Content may be subject to copyright.
Better IVF outcomes following improvements in laboratory
air quality
Rabea Youcef Khoudja & Yanwen Xu & Tao Li &
Canquan Zhou
Received: 19 September 2012 / Accepted: 19 November 2012 /Published online: 16 December 2012
The Author(s) 2012. This article is published with open access at
Background It has been proved that air quality is crucial for the
success of IVF because of the presence of volatile organic
compounds (VOCs), microbes, and perfumes, all of which
can be harmful to embryo development in vitro. Therefore
IVF laboratories are equipped with high efficiency particulate
air (HEPA), and activated carbon filters plus positive pressure
for air particulate control, with or without CODA system. Here
we introduce a new technology using specially treated Honey-
comb matrix media aligned in the Landson series system for
our laboratory air purification and its impact on IVF outcome.
Methods Air samples were collected outside and inside the
laboratory, and intra-incubator at three different time points,
before and after changing carbon filters and after Landson
system installation, and we correlated air compounds mea-
sure v ariation with IVF outcome from 1403 cycles.
Results An improvement of air quality was confirmed with
passages of total VOCs from 0.42 mg/m
, 30.48 mg/m
9.62 mg/m3, to 0.1 mg/m
0.07 mg/m
, outside the laboratory,
inside laboratory and intra-incubator respectively at three sepa-
rated air sampling times. A clear decrease was observed in some
VOCs such as formaldehyde, ethylene, acethylene, propylene,
SO2, pentane, NOx, benzene, Hallon-1211, CFC and alcohol.
At the same time a significant difference (P<0.05) was
found between the third testing time TT3 after carbon filter
change and Landson system installation and the first testing
time TT1 before carbon filter change in fertilization rate
83.7 % vs 70.1 %, embryo cleavage rate 97.35 % vs 90.8 %,
day 5 blastocyst formation rate 51.1 % vs 41.7 %, and preg-
nancy/implantation rates 54.6 %, 34.4 % vs 40.6 %, 26.4 %.
Conclusion Air purification by the new technology of Land-
son series significantly improved IVF laboratory air
quality, and embryo quality, thus increased pregnancy and
implantation rates.
Keywords Air quality control
IVF laboratory
Pregnancy rate
Implantation rate
Creating an optimal environment for embryo culture is impor-
tant for ensuring embryo viability, and thereby maintaining
stable pregnancy outcome. Various factors, such as air quality,
temperature, and light, are known to affect oocytes and embryos.
Air quality, in particular, is easy to overlo ok when pregnancy
rates start to decline. Volatile organic compounds (VOCs) are
very harmful to embryos [1]. During embryonic growth and
development, VOCs directly attach to DNA and abort growth
[24] found that episodic air pollution is associated with in-
creased DNA fragmentation in human sperm without other
changes in semen quality . Many studies have also documented
that small amounts of VOCs in the circulating air of an IVF
laboratory can have detrimental effects on pregnancy rates [5, 6].
It has been well documented that the ambient air of IVF
laboratories carries harmful VOCs (e.g. styrenes, formalde-
hydes, glutealdehydes, toluene, etc.), malignant microbes,
perfumes, deodorants, and even odors from the outside envi-
ronment, which affect embryonic development [79]. Air
contaminants, such as chemical air contaminants (C ACs)
Capsule We developed a novel air purification method utilizing
specially treated honeycomb matrix media with a LandsonTM system,
which significantly improved IVF laboratory air quality, and resulted in
better embryo quality, and higher pregnancy and implantation rates.
R. Y. Khoudja
Y. X u
T. Li
C. Zhou (*)
Reproductive Medicine Center, The First Affiliated Hospital of
SUN Yat-sen University, 58 Zhongshan Road II,
Guangzhou, China 510080
J Assist Reprod Genet (2013) 30:6976
DOI 10.1007/s10815-012-9900-1
and VOCs, which are introduced from various sources, may
interact with samples, tissues, media, and oil, and consequent-
ly, have serious effects on IVF outcome [5, 10, 11, 12]. Thus,
it is essential to set-up an air filtration/purification system that
is efficient, quiet, affordable, and has the ability to filter
hydrocarbon pollutants, VOCs, and chemically active com-
pounds, and thereby eliminate airborne pathogens [13, 14].
Due to the growing amount of evidence suggesting that air
contaminants can affect IVF outcome, cleanroom specifications
for particulate and microorganism contamination in IVF labo-
ratories have been enforced by European Union laws under
Directive 2006/86/EC [15]. However, the removal of these
contaminants would require very advanced air handling sys-
tems [16]. High efficiency particulate air (HEPA) and activated
carbon filters, positive pressure, and general sterility precau-
tions can prevent contamination . Specifically, the outside air
brought into the unit is first filtered with activated carbon,
which removes various hydrocarbons, and then HEPA removes
the particulate material s (0.3microns). Furthermore, the carbon-
activated air filtration (CODA) system was introduced in 1997.
It consists of a CODA incubator filtration unit, which is used
within the incubator and environmental chamber, a CODA
and Tri-Gas inline filter, which is used as the incoming
gas lines, and the CODA tower , which filters the air in the
laboratory, procedure rooms, and working environment. Nu-
merous studies have demonstrated improvements in pregnancy
and implantation rates after using the CODA system [17, 18].
Recently, we applied a novel air purification technology in
our laboratory to remove airborne molecular contaminants
(AMCs), chemical air contaminants (CACs) and volatile or-
ganic compounds (VOCs) in order to improve the air quality
in our laboratory, using a specially treated honeycomb matrix
media (MeadWestvaco Corporation) aligned in Landson
series system (Sinolandy. Technology Company); which is
commercialized for IVF laboratory air filtration equipment
applying an optimized air dynamic and potential chemical
catalytic mechanism for air intake, pre-filter section, Mead-
Westvaco honeycomb File, power system, and post-filter pro-
tection, and an inline gas separator t o purify the intra-
laboratory air, and was installed inside our laboratory.
Thus, the aim of the present study was to assess the
impact of this novel technology on laboratory air quality
by VOC concentration changes, as well as embryogenesis
parameters (i.e. fertilization, cleavage, and embryo quality),
and pregnancy and implantation rates, before and after the
installation of the novel air filtration system.
Materials and methods
Our laboratory is approximately 130 m
, and was previously
equipped with a HEPA air filtration system with activated
carbon filters, one Gen X CODA tower laboratory air
cleaner, two Low-Boy CODA, one CODA Aero, and CO-
DA filters in some incubators, which were changed every 3
6 months. On August 10th, 2011 we installed a new intra-
laboratory air filtration system (i.e. Landson system)
while maintaining the previous components. The last
change in carbon filters was on August 2010.
Following the changes to the air filtration system, we
assessed various emb ryogenesis parameters (i.e. fertiliza-
tion, day 3 embryos cleavage, blastocyst formation, preg-
nancy, and embryo implantation rates) in our laboratory at
three separate testing times (TT). They were as follows: i)
TT1 was between April 1 and May 25, 2011, which was
prior to the carbon filter change, and thus the first air sample
was collected on May 25th; ii) TT2 was between May 25
and August 10, 2011, which was after t he carbon filter
change (i.e. May 25), but prior to the installation of the
new Landson system, and thus, the second air sample
was collected on June 10th; and TT3 was between August
11 and October 10, 2011, which was after the installation of
the Landson system on August 10th, and thus, the third
air sample was collected on August 18th. Furthermore, these
air samples were collect ed from three different pl aces,
namely the air in the hallway outside of the laboratory,
which is supplied by an unfiltered air system, the air in the
laboratory, and the air inside the same incubator. The air
sampling time was 2030 min in duration, and 100 L of air
were collected into a Tedlar bag for analysis. using high
performance liquid chromatography (HPLC) for aldehydes,
gas-chromatography/mass spectrometry with an EnTech
cryoconcentration system for VOCs, and GE online analyz-
er for nitrogen oxides (NOx) and sulfur dioxide (SO2).
Patients that underwent consecu tive standard in vitro fertil-
ization (IVF) and intra cytoplasmic sperm injection (ICSI)
cycles at the R eproductive Medicine Center of the First
Affiliated Hospital, Sun Yat-Sen University between April
1and October 10 , 2011 were included in the study, and
divided into three groups, according to the three testing
times. The inclusion criteria were as follows: <38 years
old, 4 oocytes retrieved, less than 3 IVF cycles, and un-
derwent a gonadotropin-releasing hormone agonists
(GnRH-a) long proto col.
Assessment of fertilization and embryo quality
Embryogenesis parameters, as well as normal fertilization,
cleavage, blastocyst formation, pregnan cy, and implantation
rates, were compared between the three groups (i.e. testing
time). Normal fertilization was characterized by two visible
and distinct pronuclei and two polar bodies. The day 3 (D3)
embryo grade score was evaluated on the third day after
70 J Assist Reprod Genet (2013) 30:6976
oocyte recovery, based on the modified criteria of Ziebe et
al. [19]. One to three embryos were transferred on day 3 or
5, depending on the age and cycle number, and good quality
supernumerary embryos were cryopreserved.
Pregnancy testing
Biochemical pregnancies were defined as a positive with a
urine β human chorionic gonadotrophin (β-HCG) pregnan-
cy test 18 days after follicle aspiration. Clinical pregnancies
were confirmed by ultrasound at 78 weeks of gestation,
and pregnancies were considered to be ongoing when there
was at least one fetus with a vital heartb eat after 12 weeks of
Statistical analysis
Baseline characteristics (continuous data) are presented as
mean and standard deviation (mean ± SD). Cate gorical
variables are presented as absolute counts and percentages.
Differences in fertilization, embryo cleavage, blastocyst for-
mation, pregnancy, and implantation rates were determined
via Pearsons chi-squared test and a Yates continuity cor-
rection or a Fishers exact test followed by a Bonferroni
multiple comparisons test, where appropri ate. A logistic
regression analysis was performed to determine the influ-
ence of potential confounding variables (i.e. baseline char-
acteristics) on the primary outcome. P<0.05 was considered
as stati stically significant. Statistical analyses were con-
ducted wi th the SPSS statistical package (version 19.0) for
Windows (IBM.SPSS Inc., USA).
Air contaminants
There was a total of 49 compounds detected, which included
one forma ldehyde, two acids, 37 hydro carbons and aro-
matics, and nine halogens. The total amounts of VOCs
measured in the first air sample obtained from the hallway,
laboratory, and incubators were 0.42, 30.48, and 9.62 mg/
, respectively. These levels declined to 0.10, 2.50, and
2.19 mg/m
, respectively, in the second air sample obtained
16 days after the activated carbon filters were changed, and
further decreased to 0.07, 0.16, and 0.29 mg/m
, respec-
installation of the Landson system. The VOCs that
decreased significantly from the first to the third sam-
pling time point are presented in Table 1 Therewereno
or minimal changes observed in propylene, propane,
heptane, xylene, cyclopentane, ethylbenzene, styrene
and other molecule amounts.
Clinical assessments
Of the 1403 patients that wer e included in the study, 1188
received a fresh embryo transfer, the relevant demographic
data, including age, infertility time, clin ical data, oocytes
retrieved, and enbryos transferred, are presented in table 2.
Using logistic regression analysis, it was found that there
were no significant correlations between the various poten-
tial confounding variables (i.e. age, baseline hormone lev-
els, stimulation protocol, total dose of gonadotropin, days of
stimulation, mean oocytes retrieved, and mean embryos
Table 3 presents the total fertilization rates, normal fer-
tilization rates, cleavage rates, blastocyst formation rates,
abortion rates, pregnancy rates, and implantation rates of
the three groups. Fertilization rates at TT3 and TT2 were
significantly higher than at TT1 (83.7 and 82.3 % vs.
70.1 %), and there were no significant differences found
between TT2 and TT3. The normal fertilization rate at TT3
was significantly higher than both TT2 and TT1 (66.3 % vs.
64.6 and 61.3 %; P<0.05). There was also a significant
difference between TT1 and TT2 (P<0.016). D3 embryo
cleavage rate was calculated for the all normal fertilized
embryos (2pronucleus: 2PN), and it was found that there
was a significant difference betw een TT3 cleaved embryos
and those of TT1 and TT2 (97.3 % vs. 90.8 and 94.1 %).
There were also significant differences between TT1 and
TT2 with respect to cleavage rate. Day 5 blastocyst forma-
tion rate had also evaluated at each testing time. At TT3, 499
blastocyts formed from 977 cultured embryos (51.1 %)
compared to 41.7 and 38.1 % at TT1 and TT2, respectively
(P<0.05). Furthermore, there was a decline in blastocyst
formation rate noted at TT2 compared to TT1; however, it
was not statistically significant.
A total of 173 pregnancies were successful from 317
fresh embryo transfers (54.6 %), and 248 gestational sacs
were observed via ultrasound examination at 7 weeks after
embryo transfer with an implantation rate of 34.4 % (248/
721) in the TT3 group, which was significantly higher than
that of the TT1 group (26.4 %; 240/910). There were no
significant differences in pregnancy rates between TT2 and
TT3, and implantation rates between TT1 and TT2 (Fig. 1).
However, there were significant differences in pregnancy
rates between TT1 and TT2 (29 vs. 46.7 %), and implanta-
tion rates between TT2 and TT3 (28.6 vs. 34.4 %). There
were no significant differences between groups in regards to
the abortion rate.
VOCs are detrimental to the success of IVF laboratories.
VOCs are hydrocarbon-based compounds that are emitted
J Assist Reprod Genet (2013) 30:6976 71
Table 1 level of some VOC in different areas, on different sampling time
VOC μg/m
First sampling Second sampling Third sampling
hallway lab Incubator hallway lab Incubator hallway lab Incubator
Acetylene 1.92 2.56 3.25 4.34 4.68 5.72 2.16 1.31 1.98
0.96 1.11 1.42 1.42 1.07 0.79 0.71 0.29 0.46
Pentane 2.87 3.56 3.8 6.91 5.86 5.5 0.9 1.48 1.6
NOx 17.29 12.72 12.98 11.96 6.8 7.4 10.6 6.28 7.0
Benzene 6.36 5.12 7.17 2.8 2.3 2.1 0.87 1.35 1.76
Halon-1211 303 24609 9390 26 2317 1986 23 51 113
CFC11 2.13 2.75 2.26 1.47 1.45 1.4 0.5 0.6 0.8
CFC12 3.27 5.36 4.09 4.46 3.86 3.7 1.32 1.43 1.23
CFC13 0.97 1.16 1.1 0.73 1.3 0.65 0.26 0.28 0.36
Alcohol 59.63 5792 140 3.97 141.8 119.86 8.79 73.57 79.22
Formaldehyde 13.05 13.47 8.58 13.68 10.7 9.68 6.35 8.78 9.54
Ethylene 0.07 0.56 1.15 0.75 0.83 6.46 0.24 1.1 4.62
Acethylene 1.92 2.56 3.25 4.34 4.86 5.72 2.16 1.31 1.98
Ethane 0.39 0.96 2.96 1.09 0.82 0.15 0.31 0.15 1.14
Propylene 0.53 1.42 7.78 1.45 1.37 7.93 0.34 0.6 18.74
Isobutene 6.32 8.96 9.99 10.19 6.58 6.4 1.22 1.58 3.01
Cis-butene 0.13 0.27 0.85 0.6 0.5 0.56 0.19 0.14 0.12
Cyclopentane 0.37 1.52 1.56 0.22 0.73 0.40 0.3 0.25 0.36
Table 2 Patient baseline char-
acteristics and cycle parameters
Item (mean ± SD) TT1 TT2 TT3
Patients included (n) 446 573 384
Routine IVF cycles 277 310 193
ICSI cycles 144 230 160
Half-ICSI 25 33 31
Total ET 396 475 317
D3 ET 383 420 281
D5 ET 13 55 36
Female age (years) 30.5±3.4 (2237) 30.3±3.4 (2037) 30.5±3.8 (2137)
Infertility time (years) 4.4±2.8 4.4±2.7 4.3±2.9
Days of stimulation 10.3±1.8 10.6±4.6 11.2±1.9
Total GnRH used (IU) 2117±640 2059±640 2185±761
Basal-FSH (IU/ml) 5.7±1.7 5.7±1.4 5.7±1.4
Basal-LH (IU/ml) 3.5±2.5 3.4±1.9 3.4±1.7
Basal-E2 (pg/ml) 35.4±17.4 32.8±14.8 34.2±15.6
Basal-T (nmol/l) 0.7±0.4 0.6±0.4 0.6±0.3
HCG day FSH (IU/ml) 13.7±4.6 12.8±4.8 12.7±5.6
HCG day E2 (pg/ml) 2924±1293 3154±1224 3308±1341
HCG day LH (IU/ml) 0.85±0.6 0.92±2.1 1.1±3.2
HCG day P (ng/ml) 0.6±0.3 0.6±0.4 0.6±0.4
Mature follicle (>18 mm) on HCG day 6.1±2.8 6.9±2.7 7.5±2.4
HCG day endometrial thickness (mm) 11.3±2.4 11.3±2.6 11.4±2.4
No of retrieved oocytes 6186 8210 5953
Mean no. of oocytes 13.9±7.4 14.5±7.5 15.6±7.6
Transferred embryos 910 1053 721
Mean of transferred embryos 2.3±0.5 2.2±0.5 2.2±0.5
72 J Assist Reprod Genet (2013) 30:6976
by various industries, vehicles, and heat exhausts, as well as
by a variety of cleaning products, instruments, such as
microscopes, television monitors, compu ters, and furniture.
Additionally, due to their manufacturing proces s, perfumes,
aftershave, and other highly scented aerosols may also re-
lease VOCs. Any new construction materials (e.g. paint) and
furniture also release VOCs. New furniture made, in part,
from particle board can emit VOCs, as it consists of 10 %
formaldehyde resin, which is capable of emitting gasses
over 20 years. Consequently, unexpected sources of VOCs
are commonly found in IVF laboratories. These can include
cleaning agents, perfum es, cabinets, grease on the wheels of
equipment, sources in heating ventilating and air condition-
ing (HVAC) equipment, and many stainless steel cabinets,
which typicall y have a 3/4 inch thick piece of particle board
used under the steel to provide rigidity to the countertop
High levels of VOCs (over 1 ppm) are directly toxic to
embryos, as determined via murine and human experiments
[20]. VOC levels around 0.5 ppm will typically allow for
acceptable blastocyst development and reasonable pregnan-
cy rates, but unfortunately, there are a high percentage of
miscarriages. Ideally, VOC levels should be below 0.2 ppm,
but preferably zero. Cohen et al. [8] found that after moving
their IVF laboratory, their pregnancy rates dropped signifi-
cantly due to high levels of VOCs. They also had a drop in
their pregnancy rates when a neighbor in the building
replaced their vinyl floor, which requi res the use of large
Table 3 Embryogenesis parameters and IVF outcomes measures
Item TT1 TT2 TT3 Pvalue
OPU cycle 446 573 384
ET number 396 473 317
Retrieved oocytes 6186 8210 5953
ET embryos 910 1053 721
Fertilization rate
(%) 70.1 % (4336/6186) 82.3 % (6759/8210) 83.7 % (4984/5953) <0.001
Normal fertilisation
(2PN)(%) 61.3 % (3791/6186) 64.6 % (5303/8210) 66.3 % (3931/5953) <0.001
Cleavage rate
90.8 % (3441/3791) 94.15 % (4993/5303) 97.35 % (3827/3931) <0.001
Blastocyst culture 568 1084 977
Blastocyst formation rate 41.7 % (237/568) 38.1 % (413/1084) 51.07 % (499/977) <0.001
Pregnancy rate (PR) 40.6 % (161/396) 46.7 % (222/475) 54.6 % (173/317) 0.001
c, d, e
Implantation rate (IR) 26.4 % (240/910) 28.6 % (301/1053) 34.4 % (248/721) 0.001
c, d, e
Abortion rate 4.9 % (8/161) 6.7 % (15/222) 4.1 % (13/317) 0.38
Percentages, expressed per inseminated oocyte.
Percentage, expressed per 2PN fertilized oocyte
significantly different P<0.001 compared with d and e
No significant difference was found between: TT2 and TT3 on fertilization rate, PR and IR
No significant difference was found between: TT1 and TT2 on blastocyst formation rate, PR and IR (P>0.016)
No significant difference P>0.05
Fig. 1 IVF outcome before and
after installation of air filtration
new system
J Assist Reprod Genet (2013) 30:6976 73
amounts of adhesive (i.e. a VOC source), and thereby con-
taminated their IVF laboratory. Hall et al. [9 ] published the
mean VOC levels of various areas in seven IVF labor atories.
The mean VOC levels were 0.53 mg/m
in the outside air,
1.152 mg/m
in the air supply, 2.862 mg/m
inside the
laboratory, 2.769 mg/m
in the incubator, and 4.372 mg/
in the hallway around the laboratory. Furthermore, the
average lower limit of air quality ranged from 330 to
2240 μg/m
(±636 μg/m
). Consequently, all of these IVF
laboratories were equipped with HEPA filters, pretr eatment
with carbon filtration impregnated with potassium perman-
ganate, and over-pressure for particle control.
A number of studies have shown improved pregnancy
rates, but not embryo morphological quality, with the use of
CODA air filtration systems in human IVF laboratories [17,
21]. In one study assessing cattle IVF [18], it was found
there were no significant effects of the CODA system, as
judged by the percent cleavage and embryo quality, stage, or
development; however, the pregnancy rate was improved
significantly following the transfer of both fresh and frozen/
thawed embryos. It was speculated that there was an im-
provement in the intrinsic quality of the embryo, which was
not manifested in the morphology. Esteves et al. [22] used
inline-HEPA and carbon filters located between the gas
cylinders and incubators within the intra-incubator filtration
unit, which resulted in high cleavage rates, more good
quality embryos, higher pregnan cy rates, and low spontane-
ous abortion rates compared to using only a HEPA system
and CODA tower. Furthermore, Forman et al. [23] reported
an improvement in air quality and a decrease in VOCs ,
particulates, and aldehyde, after using a HEPA system with
high activity charcoal, a potassium permanganate filter, and
CODA. Nevertheless, some studies reported no changes in
embryo quality or implantation rate with CODA versus non-
CODA systems [24].
In China, CODA systems have been applied in the labo-
ratory environment for many years. However, in our labo-
ratory, there were no improvements in pregnancy rates
documented with the use of the CODA system. Due to the
poor air quality, high VOC levels, and the hot and humid
weather in Guangzhou, the filters may became saturated
earlier than anticipated, and thereby certain VOCs may not
be removed. We hypothesize that the summertime seasonal
elevations in temperature and humi dity may also initiate the
desorption of trapped VOCs from the carbon filters installed
in the laboratory air handling system, and reduce the ad-
sorption efficacy of the syst em [25].
On August 10, 2011, a new air filtration system, consist-
ing of specially treated honeycomb matrix media fitted into
the Landson system, was installed in our laboratory. This
novel technology made clear improvements in the air qual-
ity by reducing VOC s levels, as well as making better IVF
outcome, as determined via embryo quality, and pregnancy
and implantation rates. Total VOC levels decreased outside
(0.42, 0.10, and 0.07 mg /m
) and inside the laboratory
(30.48, 2.50, 0.16 mg/m
), and in the intra-incubator (9.62,
2.19, and 0.29 mg/m
) at three separate air sampling times
(i.e. before and after carbon filter changes, and after Land-
son system installation). Interestingly, there were also
improvements in the outside air quality expressed by the
air in the hallway during the third sampling period (TT3)
compared to TT1, which may be, in part, responsible for the
improvements in laboratory air quality. Fluctuations in out-
side air VOC levels are very important. Studies have shown
that VOC concentrations are 25 times higher in indoors
than outdoor environment and 34 times higher in winter
than summer [26]. This may be due to a number of factors,
including a low rate of air exchange, the unfilter ed outside
air may be cleane r than the HEPA-filtered labor atory air or
air obtained from incubators, and the accumulation of VOCs
derived from adjacent spaces or specific laboratory prod-
ucts, all of which complicate the situation further and make
it hard to determine the sources of contaminated air [8, 12];
Of the 49 compounds detected, certain compounds, such
as formaldehyde, decreas ed significantly between the first
and third sampling time points. Between TT1 and TT3,
formaldehyde levels decreased outside and inside the labo-
ratory, but slightly increased in the intra-incubator, but these
levels were still lower than the aldehyde levels of 57.6 μg/
found in t he exterior air and 12±26.4 μg/m
in the
incubator, as reported by Hall et al. [9]. Thus, our new
filtration system ameliorated aldehyde concentrations inside
the labor atory, but not in the intra-incubator. Formaldehyde
is one of the most common VOCs. It is an off-gas from
wood products, such as plywood or particle board, and
produced by paints, varnishes, floor finishes, and cigarette
smoking [28, 29]. Formaldehyde does not accumulate with-
in the environment, as it is broken down within a few hours
by sunlight or bacteria present in the soil or water. Thus, its
main origins in an IVF laboratory are primarily internal,
such as plastics, personnel, and furnishings.
A study on Finnish women working in laboratories at
least 3 days a week found a significant correlation between
spontaneous abortion and formaldehyde exposure. Another
study on Chinese women found abnormal menstrual cycles
in 70 % of the women occupationally exposed to formalde-
hyde compared to only 17 % in the control group. After an
earthquake hit Sichuan, China, a large number of survivors
were housed in trailers made from medium-density fiber-
board, which emitted up to 5 times Chinas maximum al-
lowable formaldehyde levels. In April, 2009, there were 100
miscarriages recorded in this community, which may have
been linked to the high exposure levels of formaldehyde
[30]. Furthermore, Hall et al. [9] found an inversely corre-
lation between mouse embryo development and different
74 J Assist Reprod Genet (2013) 30:6976
acrolein (ubiquitous aldehyde) concentrations. This is not
surprising, as both [31, 32] found that aldehyde is highly
toxic and affects all molecular mechanisms involved in cell
replication [7, 10].
In the present study, similar findings to formaldehyde
were found with respect to ethylene, acetylene, ethane,
, NOx isobutene, cis-butene, cyclop entane,
benzene, CFC-11, chloroform, carbon tetrachloride, halon-
1211, and alcohol (Table 1). Specially, there were improve-
ments in intra-laboratory air contam ination compared to the
intra-incubators, where the accumulation of these VOCs
was difficult to remove. Schimmel et al. [33]. Most of these
VOCs are primarily from internal source. Cohen et al. [8]
reported that benzene, toluene, cyclenes, and other hydro-
carbons (hexane) are highly concentrated in incubators be-
cause of the items placed in them, especially plastics.
Styrene comes from Petri dishes or other materials used in
sterile cultures. Gilligan et al. [34] Benzene is derived from
gas bottles, and its levels are elevated in incubators, but
decline with increasing distances from them. These results
coincide simultaneousl y with the significant improvements
in our laboratory parameters (e.g. fertilization, cleavage,
embryo quality, and blastocyst formation rates), and conse-
quently incre ases in pregnancy and implantation rates. This
may present concerns regarding the possible implications of
these particles on in vitro embryonic development, especial-
ly given the evidence from studies on the detrimental effects
of direct exposures of related VOCs in animal embryo
cultures [35].
In a study conducted between 2000 and 2007 on
7403 cycles, Legro et al. [35] found that exposure to an
increased level of air pollutants, especially nitrogen dioxide,
has been associated with lower likelihoods of successful
pregnancy among women undergoing IVF.
Furthermore, in our study, there was a decline in the
blastocyst formation rate during TT2 compared to TT1
(i.e. before the carbon filter change) . While this was not
statistically significant, it coincided with the clear increase
in certain VOCs (i.e. ethylene, acethylene, ethane, isopen-
tane, N-pentane, and heptane) inside the incubators and
laboratory between TT1 and TT3. Thus, this finding
requires further investigation and follow-up.
However, it should be noted that the novel air filtration
system did not appear to have any effects in reducing propyl-
ene, propane, heptane, xylene, cyclopentane, ethylbenzene,
styrene, methylpentane, methylbutene, methylchlorhexane,
chloromethane, methylcyclopentane, trichloroethylene, and
tetrachloroethylene levels.
In conclusion, there were significant improvements in air
quality with the Landson system, which coincided with
better pregnancy outcome. Further research on the funda-
mental effects of air quality on embryo development is
warranted to improve IVF outcome. Additionally, more
sensitive and optimized methodology for detecting changes
in air contaminants, such as H
S and other compounds, are
warranted to improve our understanding of pregnancy fluc-
tuations due to changes in air quality.
Acknowledgements We would like to thank Mr. Zhao Feng from
MeadWestvaco Corporation for his helpful suggestions and the dis-
cussions regarding this manuscript.
Financial disclosures This study was founded by the Key Labora-
tory of the Guangdong Province and the Natural Science Foundation of
China (81100472).
Open Access This article is distributed under the terms of the Creative
Commons Attribution License which permits any use, distribution, and
reproduction in any medium, provided the original author(s) and the
source are credited.
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... Several factors such as air quality, temperature, and light can affect embryo quality [3,4]. Volatile Organic Compounds (VOCs) are highly toxic for in vitro embryo development [5]. During embryonic development, VOCs directly bind to DNA strands and impact normal development [6,7]. ...
... Contrary to other studies, in this study, since filtered and unfiltered comparisons were evaluated simultaneously, it is thought that more promising results were obtained to increase embryo quality. Khoudja et al. observed an increase in embryo quality and birth rate, as well as a decrease in spontaneous abortions, by using a new filter system for air purification in addition to the HEPA filters they used in the laboratory [5] and stated that there would be an increase in embryo quality with the reduction of volatile organic compounds. They also verified that the main reason for the change in embryo quality was the effect of the excess formaldehyde in the CO 2 gas. ...
Full-text available
Objectives: In this study, we aimed to investigate whether carbon dioxide (CO2) used in horizontal incubators during in vitro fertilization (IVF) is pure enough and whether the addition of In-Line filters affects the stress on blastocysts and blastocyst utilization rate. Materials and Methods: To examine the effect of the purity of CO2 gas on embryo quality, two pronuclei (PN) embryos of patients younger than 35 years old and undergoing intracytoplasmic sperm injection (ICSI) were divided into two groups. Embryos in Group 1 were cultured in the incubator, which has an extra CO2 filter, whilst those in Group 2 (control group) were cultured without any additional filtering. On day 3 (D3), Day 5 (D5), embryo qualities and blastocyst utilization rates between groups were examined. Three different filters with different brands were examined regarding their effects on embryo quality within groups. For animal studies, 10-week-old female BALB/C mice (n=10) were stimulated with Follicle Stimulating Hormone (FSH) followed by Human Chorionic Gonadotropin (hCG) and mated with fertility-proven adult male mice. Mice with vaginal plaques after 24 hours were sacrificed, and 1-cell embryos were collected. Embryos were pooled first and then distributed into Group 1 and Group 2 randomly. To assess the effect of gas purity on embryonic stress, Glucose-regulated Protein 78 (GRP78) level was examined using Western blot method. Results: CO2 gas content used in IVF laboratories was not as pure as indicated, and the following impurities were isolated: ethyl methyl ketone, tetrahydrofuran, Fenol, 2-heptanol, and formaldehyde. We found that D3 embryo quality significantly improved within Group 1 compared to Group 2 (p<0,001). Similarly, when the blastocyst utilization rates were assessed, a significant increase was found in all three extra-filtered incubators compared to the ones without filters (p<0,001). Additionally, mouse embryos cultured without an extra filter have higher GRP78 expression than those cultured with an extra CO2 filter (p<0.001). Conclusion: It has been shown that the CO2 gasses used in the IVF laboratory are not as pure as reported. This can be eliminated by using an additional filter, decreasing stress and increasing embryo quality. In addition, it has been shown that the UPR plays a key role in regulating the response to ambient air/gas impurity in embryo development with long-term culture. Our study demonstrates that additional extra CO2 filters significantly improve embryo quality and impact the UPR pathway in D3 and D5 compared with a control group. This suggests that filtration of CO2 has a positive impact, perhaps by removing potentially harmful substances or affecting UPR pathways.
... Therefore, maintaining a stable laboratory environment is essential to program success. Several studies have shown that environmental contaminants (organic materials, construction dust, …) can significantly negatively impact culture and, therefore, pregnancy outcomes [1][2][3][4]. Further, it is also well established that humidity in the culture environment plays an important role in maintaining stable culture conditions [5]. However, what is less understood is the impact local seasonal weather patterns might be having on laboratory stability. ...
... Similarly, environmental exposure to VOCs and PAH adversely affects endocrine function and semen quality (sperm counts and morphology), ultimately causing reproductive issues [80][81][82]. VOCs are well known to have detrimental effects on embryo development resulting in decreased IVF success chances since they have lower implantation and pregnancy rates [83,84]. ...
Full-text available
Electronic cigarettes (e-cigarettes) are often considered a “safe substitute” for conventional cigarette cessation. The composition of the fluid is not always clearly defined and shows a large variation within brands and manufacturers. More than 80 compounds were detected in liquids and aerosols. E-cigarettes contain nicotine, and the addition of flavorings increases the toxicity of e-cigarette vapour in a significant manner. The heat generated by the e-cigarette leads to the oxidation and decomposition of its components, eventually forming harmful constituents in the inhaled vapour. The effects of these toxicants on male and female reproduction are well established in conventional cigarette smokers. Although toxins were measured at much lower levels in e-cigarette aerosols compared to smoke from a conventional cigarette, there are concerns about their potential impact on male and female reproduction. The information available was mainly obtained from studies conducted in animal models, and investigations in humans are scarce. However, the effects observed in animal models suggest that caution should be taken when vaping and that more research needs to be conducted to identify its potential adverse effects on fertility. The prevalence of e-cigarette usage is alarming, and warnings should be made about the impact of vaping on reproductive health. This document reviews the data regarding the impact of e-cigarette use on male and female reproduction.
... The IVF laboratory essentially plays the role of a mother in the womb by promoting an optimal safe condition and a robust support system for developing embryos. Therefore, developing embryos need an ideal pathogen-free environment once out of the incubator (Curchoe et al., 2020; Khoudja et al., 2013). IoT (Internet of Things) devices and sensors provided a better opportunity to control and maintain the internal environment of the IVF lab (Marques and Pitarma, 2019). ...
Full-text available
During the last few decades, assisted reproductive technologies (ARTs) have flourished rapidly and accompanied a set of advanced procedures such as intracytoplasmic sperm injection (ICSI), electronic witnessing, digital monitoring through embryoscope time-lapse systems, consistent decision-making algorithms with advanced statistics modes and preimplantation genetic testing (PGT). In usual practice, manual procedures were routinely used in IVF (in vitro fertilization) laboratories worldwide, but automation and artificial intelligence (AI) systems are promising techniques for quality assurance, which reduced the burden on the working staff in the embryology laboratory. In addition, these systems are equipped with powerful mathematical tools that minimize technician variability in the IVF lab and efficiently generate data for impaired gametes and embryos. The principal challenge of single-sperm selection out of 108 gametes can be sorted out by incorporating machine learning algorithms coupled with advanced data processing capabilities. In the same line, the emergence of closed embryo culture systems (CECSs) in human embryology has enabled the accurate morphokinetic evaluation of the more rapid cell division and the identification of normal and abnormal hallmarks of embryo viability. In particular, these CECSs are guided by the latest time-lapse microscopy (TLM) facility to continuously monitor embryo development kinetics without removing them from controlled and stable incubator conditions. In conclusion, AI-driven models can reduce technical variability in sample handling and remove the burden of the most subjective, tedious and/or monotonous aspects of the IVF lab. Furthermore, these systems also highlight environmental stressors that could hamper embryo development competence. In a broader sense, AI-based approaches are more accurate, precise and rapid in predicting embryo quality noninvasively.
... Most IVF clinics use ethanol as a disinfectant which is a known type of VOC. To overcome this, adequate air filtering is required in the IVF laboratory which can filter out hydrocarbon pollutants, chemically active components, and pathogens [18]. ...
Full-text available
Background and Objectives: The Ministry of Health as a national authority and several international organizations highly recommend that each IVF clinic conduct reviews for service regulations, and make adjustments for the patient's services according to the COVID-19 pandemic. A survey of IVF clinic management in Indonesia during the COVID-19 pandemic needs to be carried out so that the results of the survey can be used as evaluation material for the management to improve services safely. Methods: This cross-sectional survey was conducted among 49 IVF laboratory staff members of ISHE from 42 IVF clinics in Indonesia. We administered an online questionnaire containing several questions related to the management of IVF clinic services during the COVID-19 pandemic based on a search of scientific literature. Results: Several services adjustments have been made by IVF clinic management in response to the COVID-19 pandemic to minimize transmission of the virus in the IVF clinic. The IVF clinic management revised the service regulations and the patient services procedure was also undergone several adjustments, to minimize the COVID-19 transmission. Conclusions: Several adjustments were made by IVF clinic management in Indonesia as an early response to the COVID-19 pandemic. Clinic managements compile several adjustments to the service regulations during the COVID-19 pandemic as one of the readiness of IVF clinics in providing safe services for patients and staff
... Việc nuôi cấy kéo dài từ 5 đến 6 ngày sau thụ tinh giúp tăng cơ hội sàng lọc phôi, tăng kết quả có thai so với chuyển phôi giai đoạn phân cắt. Việc nuôi cấy phôi nang đòi hỏi điều kiện nuôi cấy có độ ổn định cao và quản trị nghiêm ngặt để hạn chế các yếu tố có thể ảnh hưởng đến chất lượng phôi [2,7,9,12]. Bên cạnh đó, chất lượng giao tử là yếu tố quyết định chất lượng phôi nang, đặc biệt là chất lượng noãn. ...
Objective: This study aimed to evaluation of formation and development of blastocyst in in-vitro fertilization in women with polycystic ovary syndrome. Methods: Retrospective study on 53 women with PCOS and 52 women with non-PCOS, who underwent in-vitro fertilization with blastocyst culture at Center for Reproductive Endocrinology and Infertility, Hue University of Medicine and Pharmacy Hospital since January 2019 until December 2020. Results: In women with PCOS, ovarian stimulation resulted in a greater number of retrieved oocyte and blastocyst embryos. Study group with PCOS had a statistically significant lower fertilization rate and day-5 embryo rate of 74.8% and 54% compared with those in the control group (84% and 61.2%, respectively). No statistically significant differences were observed in the mature oocyte rate, the good cleavage embryo rate and the pregnancy rate in the group with PCOS compared with the control group. Conclusion: Women with PCOS have higher number of retrieved oocytes after stimulation. The ability to fertilization and quality of blastocyst was lower in the group with PCOS but the potential for implantation and pregnancy rate were similar to the control group after vitrified-warmed embryo transfer. Key words: Polycystic Ovary Syndrome (PCOS), blastocyst, in vitro fertilization, infertility
... Ebner 27 and his colleagues reported that children born with fetal malformation rate with embryos classified as C and D are respectively 13.3 and 36.4%. It can be possibly explained by the higher degree of apoptosis, chromosomal disorder 32 and regulatory proteins loss [28][29][30] . ...
... Nevertheless, this is the first report to indicate off-gassing plasticware as a standard procedure for IVF laboratories and to introduce the hatching rate as a new variable for MEA. Many laboratories and unpublished data have suggested off-gassing plasticware allows materials such as aldehydes, toluene, cyclenes, styrene, and other hydrocarbons to dissipate and have decreased presence in embryo culture Khoudja et al., 2013). ...
Objective: To determine if reproductive toxicity might be reduced by off-gassing plasticware before use in in vitro fertilization culture. Methods: Petri dishes were grouped according to the off-gassing days before use for testing as follow: 0 day (Group A); 3 days (Group B); 7 days (Group C). Two bioassays were run: Human survival sperm assay (HSSA) at 24 hours for all groups and mouse embryo assay (MEA) to evaluate the effect of the off-gassing procedure. Sperm motility and sperm motility index values were examined and blastocyst formation was calculated on Days 4 and 5. Results: HSSA revealed decreased sperm motility in Group A (84%) compared to Groups B (94%) and C (93%) (p<0.5). MEA showed no statistical difference in blastocyst formation for the off-gassing groups (79.6%, 84.4%, 80%, Group A, B, and C, respectively; p>0.5). Hatching blastocyst formation on Day 5 was decreased in the nonoff- gassing group (49% vs. 56.7%, p>0.5). Conclusions: Off-gassing for at least 72 hours decreases the toxicity of plasticware before use in in vitro fertilization cultures for HSSA. Further investigation needs to be done in order to standardize the bioassays used to evaluate this procedure.
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Objective To evaluate the effect of air pollution, from oocyte retrieval to embryo transfer, on the results of in vitro fertilisation (IVF) in terms of clinical pregnancy rates, at two fertility centres, from 2013 to 2019. Design Exploratory retrospective cohort study. Setting This retrospective cohort study was performed in the Reproductive Biology Department of Bordeaux University Hospital localised in Bordeaux, France and the Jean Villar Fertility Center localised in Bruges, France. Participants This study included 10 763 IVF attempts occurring between January 2013 and December 2019, 2194 of which resulted in a clinical pregnancy. Primary and secondary outcome measures The outcome of the IVF attempt was recorded as the presence or absence of a clinical pregnancy; exposure to air pollution was assessed by calculating the cumulative exposure of suspended particulate matter, fine particulate matter, black carbon, nitrogen dioxide and ozone (O 3) , over the period from oocyte retrieval to embryo transfer, together with secondary exposure due to the presence of the biomass boiler room, which was installed in 2016, close to the Bordeaux University Hospital laboratory. The association between air pollution and IVF outcome was evaluated by a random-effects logistic regression analysis. Results We found negative associations between cumulative O 3 exposure and clinical pregnancy rate (OR=0.92, 95% CI = (0.86 to 0.98)), and between biomass boiler room exposure and clinical pregnancy rate (OR=0.75, 95% CI = (0.61 to 0.91)), after adjustment for potential confounders. Conclusion Air pollution could have a negative effect on assisted reproductive technology results and therefore precautions should be taken to minimise the impact of outdoor air on embryo culture.
Full-text available
The in vitro embryo production (IVEP) technique is widely used in the field of reproductive biology. In vitro maturation (IVM) is the first and most critical step of IVEP, during which, the oocyte is matured in an artificial maturation medium under strict laboratory conditions. Despite all of the progress in the field of IVEP, the quality of in vitro matured oocytes remains inferior to that of those matured in vivo. The accumulation of substantial amounts of reactive oxygen species (ROS) within oocytes during IVM has been regarded as one of the main factors altering oocyte quality. One of the most promising approaches to overcome ROS accumulation within oocytes is the supplementation of oocyte IVM medium with antioxidants. In this article, we discuss recent advancements depicting the adverse effects of ROS on mammalian oocytes. We also discuss the potential use of antioxidants and their effect on both oocyte quality and IVM rate.
Latex paints are widely used in residential and commercial indoor environments. The surface areas covered by the paints in these environments are relatively large. Thus, latex paints have the potential for having a major impact on indoor air quality (IAQ). A study was undertaken to develop methods for evaluating the impact of latex paint emission on IAQ. Small chamber experiments using stainless steel and painted and unpainted gypsum board substrates were conducted to determine the emission characteristics of latex paint. The emissions from the stainless steel were relatively short lived (3 to 4 days), whereas the emissions from gypsum board lasted for over 200 days. Because gypsum board is a common substrate for latex paint, all emission models were developed for the gypsum board substrates. The data from the small chamber tests led to the development of two empirical and two mass-transfer-based source emission models. Approximately 100 to 200 days of data were required to estimate the parameters required for the empirical models. Only 8 days of data were required to estimate the parameters for the mass-transfer-based models. The final models use paint formulation and mass transfer correlations to predict the emissions of the major individual volatile organic compounds emitted by latex paint.
This comprehensively updated and expanded second edition builds on its successful and popular predecessor, retaining the practical features which made the first edition such an essential guide to IVF. The edition describes additions to the range of ART clinical treatments, including the use of testicular and epididymal sperm, blastocyst stage transfer, and new perspectives in cryobiology and cryopreservation techniques. By incorporating laboratory techniques and protocols, with an even greater emphasis on quality control, it provides an indispensable and practical account. The introductory chapters covering the scientific background that underpins effective laboratory practice have been substantially expanded, derived from research in mammalian systems into the molecular biology of oogenesis, oocyte maturation, and early embryo metabolism. This second edition distils a wealth of practical and scientific detail for the benefit of all IVF practitioners.