Journal of Chemical Health Risks

Journal of Chemical Health Risks (2015) 5(2), 7380

ORIGINAL ARTICLE

Investigation of Polychlorinated Dioxins, Furans

(PCDD/Fs)
and
Dioxin-like
Polychlorinated
Biphenyls (dl-PCBs) in Human Milk
Aldo Pacheco Ferreira*, Sergio Rabello Alves
Oswaldo Cruz Foundation, Sergio Arouca National School of Public Health, Center for the Study of Workers
Health and Human Ecology, Rio de Janeiro, Brazil
(Received: 11 Junuary 2015

Accepted: 12 March 2015)

ABSTRACT: A study on polychlorinated dibenzo-p-dioxins (PCDDs), polychlorinated

dibenzofurans (PCDFs) and dioxin-like polychlorinated biphenyls (dl-PCBs) was conducted in a

KEYWORDS

pooled sample of breast milk from 27 first-time mothers (primiparous) living in twelve locations at
Human milk

mesoregion industrial area, southern of Rio de Janeiro, Brazil, between August 2012 and July

Body burden

2014. Questionnaires with questions regarding to food habits, social and economic conditions,

Polychlorinated
dibenzo-p-dioxins and

places of dwelling were applied. Mothers were breast-feeding only one infant and milk was

dibenzofurans

collected between 4 and 6 weeks after delivery. TEQs of PCDDs/Fs, and dl-PCBs were 10.6, 4.77,

Dioxin-like

6.96 TEQ pg/g, respectively. The understanding and identification of pollution sources may be

polychlorinated

helpful for taking better counter measures against breast milk dioxin contamination. Its important

biphenyls
Risk assessment
Public health

for pregnant women to have a diet free as possible of contaminants chemical. Further research
must be undertaken in the context of epidemiological investigations to more accurately assess the
effects of these compounds.

INTRODUCTION
Contaminations by polychlorinated dibenzo-p-dioxins

contain high levels of these compounds. These

(PCDDs), polychlorinated dibenzofurans (PCDFs) and

compounds bio-accumulate in humans mostly through

dioxin-like polychlorinated biphenyls (dl-PCBs) are

food, particularly from fish, meat and milk. The

closely related groups of chemical byproducts that are

elimination of these compounds from body fat is very

produced and distributed throughout the world [1].

slow. Due to the relatively high fat content of breast

Due to their persistence and lipophilic character, they

milk, these compounds are transferred into the milk.

tend to become concentrated in the food chain.

The levels in milk are strongly correlated with the fat

Humans are at the top of food chain, so human tissues

content

Corresponding author: aldopachecoferreira@gmail.com (Aldo Pacheco Ferreira).

of

the

milk

and

influenced

by

the

A. Pacheco Ferreira and S. Rabello Alves/ Journal of Chemical Health Risks 5(2) (2015) 7380

concentration of adipose tissue [2]. Infants are

preservative pentachlorophenol, and the phenoxy

exposed to PCDDs/Fs, and dl-PCBs prenatally and

herbicides), or working in industries that produce

via breast milk [1-3]. Chemically stable and lipophilic

dioxin and furan byproducts [12].

properties of these contaminants led to their high

Dietary exposure makes up more than 90 percent of

contamination in higher trophic biota, including

human dioxin and furan intake [4]. Fatty foods usually

human [2,3]. Despite the intensive monitoring efforts

contain more significant levels because they are higher

and anticipated results of decreasing trends of

on the food chain and thus have accumulated more

PCDDs/Fs and dl-PCBs in developed countries as a

dioxin. Once dioxins and furans have entered animal

consequence of their regulation on use and waste

tissues, they have few avenues of departure, so the

treatment, little information are available on their

chemicals can persist for many years. In lactating

contamination status in developing countries even

women, dioxins and furans may leave the body in

though these chemicals are still being used and

breast milk. As with many other persistent chemicals

unintentionally produced in several parts of these

that appear in breast milk, the concentration of dioxins

countries.

and furans changes with time [9, 12].

Dioxins and furans are among the most hazardous

A number of animal and human studies have looked at

chemicals known - extremely tiny doses have been

the health effects of dioxins and furans on children's

shown to cause negative health effects [4]. These

health from in utero and postnatal exposure. Health

chemicals are listed by several governmental agencies

outcomes evaluated have included low birth weight,

as known causes of cancer in humans [5]. A small

hormone fluctuation, neurobehavioral function, and

share of the dioxins and furans released into the

altered immune function [13]. Thus, many studies

environment are broken down by sunlight, but most

have identified step-by-step links between these health

persist by attaching to soil particles and sediment in

effects and exposure to dioxins specifically from

water. Once attached to such particles, they enter the

breast milk [2, 7, 10, 11, 13-15].

food chain, leading eventually to bioaccumulation in

In order to quantify the consumption by infants of the

animal fat [6]. Indeed, studies have linked dioxins and

contaminants studied, their intake through breast milk

furans to many adverse effects on human health, such

was estimated. In fact, in many cases, human milk is

as carcinogenicity, immunotoxicity and neurotoxicity

the only food that new-borns consume in the first

[7-11]. Dioxins and furans are attracted to fat, resistant

months of life, such an analysis, therefore, makes it

to metabolism, and have lipophilic nature which

possible to estimate the intake of xenobiotics in a

allows accumulation in human tissues [2, 9]. Within

more simple and accurate manner than can be done in

the human body, the highest levels of these chemicals

organisms with a more complex diet. In this study, the

are in fat and breast milk. These compounds are lipid-

presence

soluble,

therefore

organochlorinated compounds was evaluated in

accumulated and stored in human adipose tissues.

samples of breast milk. In this paper are presented data

They can pass through the placenta causing exposure

on the levels of PCDD/Fs and dioxin-like PCBs in a

of the foetus, and their existence in human milk

pooled sample of breast milk from 27 mothers living

exposes infants during the lactating period.

at twelve locations at mesoregion industrial center of

Human beings can be exposed to dioxins and furans in

southern Rio de Janeiro, Brazil.

poorly

eliminated

and

are

a number of ways. Eating contaminated food

(primarily meat, dairy products, and fish) is the major
path for dioxin exposure [3, 5], but other less common
routes of exposure include contact with certain
pesticides

and

herbicides

(such

as

the

wood
274

and

levels

of

some

classes

of

A. Pacheco Ferreira and S. Rabello Alves/ Journal of Chemical Health Risks 5(2) (2015) 7380

combined organic phase collected was evaporated to

MATERIALS AND METHODS

dryness by the rotary evaporator with water bath at

Sampling collection

40C. The dried organic phase was weighed and

Human breast milk samples were collected from

dissolved in 5 mL hexane and then subjected to clean-

mothers living in 12 different regions at mesoregion

up procedure below. The same extraction procedure

industrial area (Angra dos Reis, Barra do Pira, Barra

was followed for the other individual milk samples.

Mansa, Itatiaia, Parati, Pinheiral, Pira, Porto Real,

Spiked samples were treated in a similar manner

Quatis, Resende, Rio Claro, Rio das Flores, Valena,

Sample extracts clean-up: The silica solid phase

and Volta Redonda), southern Rio de Janeiro, from

extraction column (500 mg / 6 mL) cartridges were

August 2012 to July 2014. A detailed questionnaire

conditioned with 10 mL petroleum ether. The organic

was given to obtain an informative record of the

layer dissolved in 5 mL hexane was cleaned up by

participants [16]. Before giving milk, each mother

shaking for 1min in 2 mL concentrated sulphuric acid.

completed an informed consent form. Breast milk

The sample extracts were loaded onto the columns and

samples were collected by manual expression and

eluted with 1: 9 diethyl ether/petroleum ether mixture.

pooling of individual samples was done on a volume

Spiked samples were treated similarly. The cleaned

basis by taking 10 ml of collected milk from each

extracts were concentrated to dryness by rotary

donor so that a final volume of 270 ml. All samples

evaporation. The dried residues were for each sample

were collected between 4 and 6 weeks after delivery.

were dissolved in 1 mL ethyl acetate and then picked

into a 2 mL vial for analysis by the gas

Sample preparation and extraction

chromatograph.

All solvents were grade of dioxin analysis and active

Analysis

carbon-impregnated silica gel was purchased from

Sigma-Aldrich (So Paulo, Brazil). Silica gel 60 was

Gas chromatography (GC) analyses were performed

purchased from Merck (Rio de Janeiro, Brazil).

on a Varian CP-3800 GC equipped with a CP-8400

autosampler and an electron capture detector (ECD).

13

C12-PCDDs, PCDFs, and dioxin-like PCBs standards

were

purchased

from

Wellington

The GC conditions used for the analysis included a

Laboratories

(Ontario, Canada).

capillary column coated with RB-5 (300.25 mm,

Fat extraction was performed using the BLH-IFF/NT-

0.25 m film thickness), a carrier gas at a flow rate of

30.05 methods [17]. The extraction of the human

1.0 mL/min and a make-up gas of Nitrogen also at a

breast milk samples procedure carried out was that

flow rate of 29 mL/min. The temperature of injector

described by Horii et al. [18]. The human breast milk

operating in splitless mode was held at 225C, oven

samples frozen at -20C were allowed to thaw and

temperature was set at 225C and electron capture

then stirred thoroughly. 10 mL of the milk samples

detector was also set at 300C. The column oven

were then pipetted and homogenised with 40 mL of

temperature was programmed as follows; 60C for 2

1:1 petroleum ether/acetone mixture by macerating the

min, 180C/min up to 300C held for 31.80 min. The

mixture with the aid of an Ultra-Turrax T 25 basic at a

injection volume of the GC was 1.0 L. The residues

speed of 9,500 rpm for 2 min to enhance extraction.

detected by the GC analysis were confirmed by the

The homogenate were then centrifuged at 2500 rpm

analysis of the extract on two other columns of

for 2 min. After centrifuging the organic layer was

different polarities. The first column was coated with

collected into an already weighed round bottom flask.

ZB-1 (methyl polysiloxane) connected to ECD and the

The milk phase was re-extracted twice with two

second column was coated with ZB-17 (58% phenyl,

separate aliquots of 30 mL petroleum ether. The

375

A. Pacheco Ferreira and S. Rabello Alves/ Journal of Chemical Health Risks 5(2) (2015) 7380

methyl polysiloxane) and ECD was also used as

concentrations was run and the detector response for

detector [19].

each compound was determined. The areas of the

corresponding peak in the samples were compared

Quantification

with that of the known standards. The detection limits

The quantities of residues in the samples were

for PCDDs, PCDFs, and dioxin-like PCBs in this

determined using an external standard method. An

study are given in Table 1. The non-detected outcomes

organochlorine

were set as zero.

standard

mixture

with

known

Table 1. Detection limits of PCDDs, PCDFs, and dioxin-like PCBs in human breast milk
PeCDD/DF

PCDDs, PCDFs

OCDD/DF

Dioxin-like PCBs

0.1 pg/g

0.03 pg/g

HxCDD/DF
HpCDD/DF
0.01 pg/g

0.05 pg/g

Calculation of the toxic equivalent (TEQ) of the

dioxin analogues in the analyzed samples were
Recovery test

calculated using the World Health Organization

(WHO)-2005 toxic equivalency factors (TEF) [20].

One sample in each batch of analysis was spiked with

The

aromatic

0.1 mL/kg of a mixed standard. The spiked samples

compounds mixtures complicates the risk evaluation

were extracted and analyzed under the same

for humans, fish, and wildlife. For this purpose, the

conditions as the samples. The recovery for the

concept of TEFs has been developed and introduced to

different organochlorine compounds in the milk

facilitate risk assessment and regulatory control of

samples were between 89 to 97%. The percentage

exposure to these mixtures. To apply this TEF

recovery was calculated as: Recovery (%) = ((Amount

concept,

of analyte received) / (Amount of analyte spiked))

complex

nature

of

fundamental

Halogenated

understanding

of

the

mechanism of action is a prerequisite. At present,

100.

there is sufficient evidence available that there is a

STATISTICAL ANALYSIS

common mechanism for these compounds, involving

binding to the aryl hydrocarbon (Ah) receptor as an

Calculations and statistical analysis were performed

initial step. When applying the TEF concept, the

using the statistical data

toxicity of these compounds relative to that of 2, 3, 7,

program Origin 7.5

(OriginLab).

8-TCDD is determined on the basis of available in

vivo and in vitro data. However, it should also be

RESULTS

understood that the TEF concept is based on a number

The donors ranged in age from 18 to 32 years

of assumptions and has limitations. In this respect, the

(median: 23 years) and all of them (27) were

most basic assumption is that the combined effects of

primiparous. All mothers have provided a detailed list

the different congeners are dose or concentration

of dietary habits. The diet of the participants did not

additive, and results of many studies support this

seem to differ much between the studied areas. It was

assumption. The toxic equivalency of a mixture is

a mixed diet with consumption of meat, fish, milk, and

defined by the sum of the concentrations of individual

dairy products. In respect to weekly food consumption

compounds (Ci) multiplied by their relative toxicity

(%), 88.9% ate meat 1-2 times a week (24), 7.4% ate

(TEF) [21].

3-5 times a week (2), and 3.7% never ate (1). In fish
TEQ = [Ci] TEFi (equation 1)

consumption (%), 44.4% ate 1-2 times a week (12),

4
76

A. Pacheco Ferreira and S. Rabello Alves/ Journal of Chemical Health Risks 5(2) (2015) 7380

18.52% ate 3-5 times a week (5), and 37.08% never

exposure to related compounds. All donors had been

ate (10). With milk consumption, it were found no

living in the study area for at least 5 years before milk

consumption

collection.

in

(14.82%),

(18.52%) 1-2

times/week, 9 (33.33%) 3-5 times/week, and 9

Tables 2 and 3 shows the levels of PCDD/Fs, and dl-

(33.33%) > 5 times/week. Most mothers were non-

PCBs congeners and total TEQs found in this pooled

smokers (80%) ranging from 70 to 90% between

sample of mothers' milk from twelve locations related

samples. From smoking mothers (20%), 7% were

to the studied area. The average TEQs of PCDDs,

smokers and 13% former smokers. No donor reported

PCDFs, dioxin-like PCBs were 10.6, 4.77, 6.96 TEQ

occupational exposure that could be associated with

pg/g fat.

Table 2. PCDD/Fs concentrations (pg/g fat) and total TEQs (TEQ pg/g fat) in a pooled breast milk samples from industrial polo, RJ, Brazil
Congener

pg/g fat

Dibenzo-p-dioxins (PCDD)
2378-TCDD

1.27

12378-PeCDD

6.19

123478-HxCDD

0.54

123678-HxCDD

22.47

123789-HxCDD

7.22

1234678-HpCDD

8.6

OCDD

77.27

Total PCDDs TEQs

10.6

Dibenzofurans (PCDF)
2378-TCDF

1.18

12378-PeCDF

0.49

23478-PeCDF

12.48

123478-HxCDF

3.31

123678-HxCDF

3.22

1234789-HxCDF

0.18

234678-HxCDF

2.02

1234678-HpCDF

1.99

1234789-HpCDF

OCDF

0.73

Total PCDFs TEQs

4.77

Total TEQs (PCDDs + PCDFs)

15.37

77
5

A. Pacheco Ferreira and S. Rabello Alves/ Journal of Chemical Health Risks 5(2) (2015) 7380

Table 3. Dl-PCBs concentrations (pg/g fat) and total TEQs (TEQ pg/g fat) in a pooled breast milk samples from industrial polo, RJ, Brazil
Congener

pg/g fat

Non-ortho PCBs
3,3',4,4'-TCB (77)

36.5

3,4,4',5-TCB (81)

24.74

3,3',4,4',5-PeCB (126)

60.7

3,3',4,4',5,5'-HxCB (169)

38

Mono-ortho PCBs
2',3,4,4',5-PeCB (123)

34.29

2,3',4,4',5-PeCB (118)

9067

2,3,3',4,4'-PeCB (105)

1842

2,3,4,4',5-PeCB (114)

891

2,3',4,4',5,5'-HxCB (167)

1034

2,3,3',4,4',5-HxCB (156)

2897

2,3,3',4,4',5'-HxCB (157)

879

2,3,3',4,4',5,5'-HeCB (189)

249

Total dioxin-like PCBs TEQs

6.96

Total dioxin TEQs

22.33

Because of this exclusively in the food and the fact

DISCUSSION AND CONCLUSIONS

that at this stage many organs are still in development,

In this survey, breast milk samples from 27 mothers
were analyzed for polychlorinated compounds. To our
knowledge, this is the most recent and extensive study

the new-borns seem to be the sector most vulnerable

on the human breast milk contamination by PCDD/Fs

to organochlorinated compounds [27]. A child who

and dl-PCBs in Rio de Janeiro, Brazil. The main

eats human milk is at the apex of the food chain and

factors influencing the levels of PCDD/FS and dl-

thus can receive a higher burden of contaminants

PCBS in human milk is the fat content, the elapsed

eliminated by this pathway, especially those capable

time from the start of lactation, age and weight of the

of undergoing the phenomenon of biomagnification

mother, parity, number of children, origin and place of

[28]. Children are particularly vulnerable to chemical

residence, eating habits, seasonality, smoking, amount

agents present in the environment due to their

of milk and occupational exposure [2, 3, 22-25].

physiological characteristics. Thus, dioxins, furans and

Generally, ingestion of contaminated food is the major

polychlorinated biphenyls in air, water, soil, food and

route of human exposure to dioxins, and accounts for

more likely to be absorbed by children than for adults

>90% of the exposure, with lower contributions from

[26, 27]. Human milk is an important vehicle for

inhalation or dermal contact [9].

elimination of xenobiotics from the body and may

Breast milk is the most complete food for newborns

constitute a source of contamination for infants [26].

because its nutritional composition is essential for the

Motivating the present study, PCDD/Fs and dl-PCBs

proper physical and mental development [26].

bioaccumulation in the food chain have been shown to

cause a number of toxic biological responses, which
78
6

A. Pacheco Ferreira and S. Rabello Alves/ Journal of Chemical Health Risks 5(2) (2015) 7380

makes exposure environmental and human focus of

Serbo

and

Jimma

in

South-Western

Ethiopia.

global concern. Especially fish, meat, and milk are

Chemosphere. 90(5), 1652-1657.

rich in dioxins due to their accumulation in tissue

7. Jensen A.A., 1983. Chemical contaminants in

lipid. While the benefits of breastfeeding outweigh the

human milk. Residue Reviews 89, 1-128

risk from contaminants in human milk, it is extremely

8. Longnecker M.P., Klebanoff M.A., Zhou H., Brock

important to continuously identify these compounds in

J.W., 2001. Association between maternal serum

breast milk. In conclusion, this study highlights the

concentration of the DDT metabolite DDE and

need of comprehensive studies on the temporal trends

preterm and small-for-gestational-age babies at birth.

of PCDD/Fs and dl-PCBs in Rio de Janeiro, Brazil, to

Lancet. 358(9276), 110-114.

understand the sources of contamination and evaluate

9. Solomon G.M., Weiss P.M., 2002. Chemical

possible long-term impacts of PCDD/Fs and dl-PCBs

contaminants in breast Milk: time trends and regional

to human health, especially to infants.

variability. Environ Health Perspect. 110, 339-347.

10. Cerrillo I., Granada A., Lopez-Espinosa M.J.,

ACKNOWLEDGMENTS

Olmos B., Jimenez M., Cano A., Olea N., Fatima

We wish to thank CNPq-Brazil for the financial

Olea-Serrano

M.,

2005.

Endosulfan

and

its

support, UFRJ and UFRGS for technical support. The

metabolites in fertile women, placenta, cord blood,

authors declare that there is no conflict of interests.

and human milk. Environ Res. 98, 233-239.

11. Winneke G., 2011. Developmental aspects of

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