Environmental Pollution 146 (2007) 225e232www.elsevier.com/locate/envpol

Organohalogen compounds in human breast milk fromRepublic of Buryatia, Russia

Oyuna V. Tsydenova a, Agus Sudaryanto a, Natsuko Kajiwara a, Tatsuya Kunisue a,Valeriy B. Batoev b, Shinsuke Tanabe a,*

a Center for Marine Environmental Studies (CMES), Ehime University, Bunkyo-cho 2-5, Matsuyama 790-8577, Japanb Baikal Institute of Nature Management, Siberian Branch of Russian Academy of Sciences, Sakhyanova st. 6, Ulan-Ude 670047, Russia

Received 27 December 2005; received in revised form 30 March 2006; accepted 12 April 2006

People in the Republic of Buryatia, Russia are exposed to relatively high levels of HCHs, HCB and PCBs.

Abstract

Human breast milk samples collected during 2003/04 in Buryatia, a Russian autonomous republic, were analyzed in order to assess humanexposure to organohalogen compounds including organochlorine pesticides, polychlorinated biphenyls (PCBs), and polybrominated diphenylethers (PBDEs). When compared with available worldwide data, levels of HCB (23e880 ng/g lipid wt.), PCBs (69e680 ng/g lipid wt.), andHCHs (100e3700 ng/g lipid wt.) were relatively high, indicating elevated human exposure to these organochlorines (OCs) in Buryatia. In con-trast to OCs, PBDE concentrations were low (0.46e1.7 ng/g lipid wt.). Out of 14 BDE congeners analyzed, BDE-28, BDE-47, BDE-100, BDE-153, BDE-197, and BDE-207 were detected. Estimated daily intakes (EDIs) of HCHs, HCB, CHLs, and PCBs by infants solely from humanmilk for 100%, 43%, 34%, and 17% of the samples, respectively, exceeded guideline thresholds. Although high EDIs raise concern for possibletoxic effects of OCs, women in Buryatia are recommended to breastfeed due to numerous advantages of breastfeeding for mother and child.� 2006 Elsevier Ltd. All rights reserved.

Keywords: Human breast milk; Organochlorines; Polybrominated diphenyl ethers; Russia

1. Introduction

Intensive usage of organochlorine (OC) pesticides in thepast and the presence of polychlorinated biphenyls (PCBs)in a number of electrical equipment in use raise concernsabout possible adverse effects on ecosystems and humans inRussia. Particularly serious concerns have been raised aboutinappropriate and excess use of OC pesticides (Fedorov andYablokov, 1999). However, information on environmental pol-lutant levels in Russia and human exposure is still limited. Fewpapers provided evidence of human exposure by reporting OClevels in human milk from Russian Arctic (Polder et al., 1998,2003) and Irkutsk region in Siberia (Schecter et al., 1990), but

* Corresponding author. Tel./fax: þ81 89 927 8171.

E-mail address: shinsuke@agr.ehime-u.ac.jp (S. Tanabe).

0269-7491/$ - see front matter � 2006 Elsevier Ltd. All rights reserved.

doi:10.1016/j.envpol.2006.04.036

the picture remains fragmentary due to vast territory of thecountry, different usage patterns between regions, and lackof time trend studies.

Another group of contaminants of interest is polybromi-nated diphenyl ethers (PBDEs), which are commonly usedas additive flame retardants. Levels of these contaminantswere shown to increase in a number of environmental com-partments and humans over the past 10e20 years (Darnerudet al., 2001; De Wit, 2002). To our knowledge, there are no re-ports on PBDE levels in Russian environment so far and thereexists no information on PBDE usage in Russia.

The area surrounding Lake Baikal is considered as rela-tively pristine as levels of OC contaminants in environmentalcompartments (air, water, sediments, soil) of the lake and ad-jacent Irkutsk region were low (Iwata et al., 1995). However,high concentrations of persistent OCs were detected in biotaof Lake Baikal, especially in Baikal seal (Pusa sibirica),

226 O.V. Tsydenova et al. / Environmental Pollution 146 (2007) 225e232

a top predator of the Lake Baikal food web (Nakata et al.,1995; Tsydenova et al., 2004). Humans, due to their uniqueposition on the pinnacle of many food chains, may be exposedto higher levels of environmental pollutants through intake ofcontaminated food. The only available evidence of human ex-posure to OC pesticides and PCBs in the Lake Baikal region isthe report by Schecter et al. (1990) who analyzed human milksamples (n ¼ 13) from the Irkutsk region adjacent to LakeBaikal on the west.

In this study, we assessed human exposure to organohalo-gen compounds using human milk from Buryatia, a regionsurrounding Lake Baikal on the east. Obtained results werecompared with data reported worldwide in order to understandmagnitude of contamination. In addition, the present studyexamined relationships between contaminant levels and age/parity of the mothers and assessed intake of contaminants byinfants through breast milk consumption.

2. Materials and methods

2.1. Sample collection

Human milk samples (n ¼ 35, including two samples with no information

about the donors) were collected in Ulan-Ude maternity hospital in December

2003 to January 2004. Location of the Republic of Buryatia and domiciles of

the donors are shown in Fig. 1. Informed consent was obtained from all the

donors. Women filled self-administrated questionnaires. Among the donors,

17 were primiparae and 16 were multiparae with average ages of 23 and

30 years, respectively. Breast milk samples were collected in solvent washed

glass containers with Teflon lined caps and kept frozen at �20 �C until

analysis.

2.2. Chemical analysis

Analyses of OCs and PBDEs were conducted following the procedures de-

scribed by Kunisue et al. (2004a) and Kajiwara et al. (2004), respectively, with

slight modifications of the latter method.

Ulan-Ude

Russia

Mongolia

Lake Baikal

Irkutsk

Buryatia

Russia

Russia

Fig. 1. Map of Buryatia showing locations of residence (:) of breast milk

donors.

For OC analysis, 10 g of human milk sample was added onto 10 g diato-

maceous earth (Extrelut NT: Merck, Germany) packed in a glass column and

extracted with 220 ml of diethyl ether. Lipid in the extract was removed by

gel permeation chromatography (GPC) packed Bio-Bead S-X 3 (Bio-Rad

Laboratories, USA). The lipid-removed extract was passed through activated

Florisil (Florisil PR: Wako Chemicals USA Inc., USA) packed in a glass

column. The first fraction eluted with hexane contained PCBs, hexachloro-

benzene (HCB), dichlorodiphenyldichloroethylene ( p,p 0-DDE) and trans-

nonachlor, and the second fraction eluted with 20% dichloromethane in

hexane contained dichlorodiphenyltrichloroethane ( p,p 0-DDT), dichlorodi-

phenyldichloroethane ( p,p 0-DDD), hexachlorocyclohexane (HCH) isomers

(a-, b-, and g-), cis-nonachlor, trans-nonachlor, cis-chlordane, trans-

chlordane, oxychlordane and tris(4-chlorophenyl)methane (TCPMe). OCs in

the first and second fractions, except TCPMe, were quantified using a gas

chromatograph (Agilent 6890 series) equipped with ECD (electron capture

detector) and an automatic injector (GC Agilent 7683 series). The concentra-

tions of individual OCs were quantified by comparing the peak area of the

particular compound in sample extracts to that of the corresponding external

standard. The PCB standard used for quantification was a mixture of 62 PCB

isomers and congeners (BP-MS) obtained from Wellington Laboratories Inc.,

Ontario, Canada. Concentrations of individually resolved peaks of PCB

isomers and congeners were summed to obtain total PCB concentrations.

For the quantification of TCPMe, a GC-MSD (Hewlett-Packard 6890 series

GC coupled with 5973 mass selective detector) was employed. Data were

acquired by a Hewlett-Packard 5973C data system, in which the cluster

ions were monitored at m/z 311, 313, 346 and 348.

For PBDE analysis, human milk sample (about 40 g) was spiked with

2 ng of internal standards (13C12-labeled BDE-3, BDE-15, BDE-28, BDE-

47, BDE-99, BDE-153, BDE-154, BDE-183, BDE-197, BDE-207 and

BDE-209) and added onto 40 g diatomaceous earth (Extrelut NT: Merck,

Germany) packed in a glass column and extracted with 250 ml of diethyl

ether. The extract, after concentration, was subjected to GPC for lipid

removal. The GPC fraction containing PBDEs was concentrated and passed

through 1.5 g of activated silica gel (Wakogel S-1: Wako Pure Chemical In-

dustries Ltd., Japan) column with 5% dichloromethane in hexane for clean

up. 13C12-labled BDE-139 was added to the final solution prior to GC-

MSD analysis. Quantification was performed using a GC (Agilent 6890N)

equipped with MSD (Agilent 5973N) for mono- to hepta-BDEs, and GC

coupled with MS (JEOL GCmate II) for octa- to deca-BDE, using an

electron impact with selective ion monitoring (EI-SIM) mode. GC columns

used for quantification were DB-1 fused silica capillary (J&W Scientific

Inc.) having 30 m � 0.25 mm i.d. � 0.25 mm film thickness for mono- to

hepta-BDEs, and 15 m � 0.25 mm i.d. � 0.1 mm film thickness for octa- to

deca-BDEs. Target congeners were BDE-3, BDE-15, BDE-28, BDE-47,

BDE-99, BDE-100, BDE-153, BDE-154, BDE-183, BDE-196, BDE-197,

BDE-206, BDE-207, and BDE-209. All the congeners were quantified using

the isotope dilution method to the corresponding 13C12-labeled congeners

[BDE-100 (penta-BDE), BDE-196 (octa-BDE), and BDE-206 (nona-BDE)

were quantified using 13C12-labeled BDE-99 (penta-BDE), BDE-197 (octa-

BDE), and BDE-207 (nona-BDE), respectively]. Recoveries of 13C12-labeled

BDEs ranged between 60% and 120%.

Procedural blanks were analyzed simultaneously with every batch of five

samples to check for interferences or contamination from solvents and

glassware. Detection limits were calculated as 3 times the procedural blank.

Lipid contents were determined gravimetrically by measuring the total non-

volatile solvent extractable material on subsamples taken from the original

extracts.

2.3. Statistical analysis

Statistical treatment of the obtained results was performed with the SPSS

software (SPSS for Windows: SPSS Inc., 2001). The ManneWhitney U-test

was used to examine differences in OC concentrations between subjects

grouped by parity. Spearman’s rank correlation coefficient was used to

measure the strength of the association between mother’s age and OC concen-

trations. Probability values less than 0.05 obtained using the ManneWhitney

U-test were considered as statistically significant.

227O.V. Tsydenova et al. / Environmental Pollution 146 (2007) 225e232

3. Results and discussion

3.1. Contamination status

3.1.1. PCBs and OC pesticidesOrganohalogen compounds were detected in all the human

milk from Buryatia (Table 1). The most abundant contami-nants were HCHs, DDTs, PCBs and HCB, whereas othercompounds such as chlordane related compounds (CHLs),TCPMe, and PBDEs were present at relatively low levels.Generally, HCHs were detected at the highest concentrations(100e3700 ng/g lipid wt.), followed by DDTs (170e1800 ng/g lipid wt.), PCBs (69e680 ng/g lipid wt.), andHCB (23e880 ng/g lipid wt.).

The distribution pattern found was similar to that observedin late 1980s (HCHs > DDTs > HCB > CHLs) in humanmilk from the neighboring Irkutsk region (Schecter et al.,1990). However, it was different from that observed in Baikalseal blubber, in which DDTs were the most abundant com-pounds followed by PCBs, CHLs, HCHs, and TCPMe (Nakataet al., 1995; Tsydenova et al., 2004). The differences in distri-bution of OCs in these two matrices, probably, reflect differentmetabolizing capacities of humans and seals or different sour-ces of exposure.

Comparison of OC levels in human milk from Irkutsk re-gion (Schecter et al., 1990) and this study allows assessmentof time trends in human exposure to OCs in the Lake Baikalregion (Table 2). Human levels of HCHs and DDTs seemedto have decreased substantially in the region over a 15-yearperiod, possibly, as a result of cessation of the use of thesepesticides. DDT usage was banned in 1970 and the use of tech-nical HCH ceased in 1986 (Fedorov and Yablokov, 1999;Zhulidov et al., 2002). HCB concentrations in the present studywere slightly lower than those in milk from Irkutsk region15 years ago, probably also reflecting the ban on agricultural

Table 1

Mean and range of concentrations (ng/g lipid wt.) of organohalogen com-

pounds in human breast milk from Buryatia

Primiparae (n ¼ 17) Multiparae (n ¼ 16)

Age 23 (18e31) 30 (23e43)

Lipid (%) 2.9 (0.91e6.2) 2.4 (0.67e7.2)

PCBs 240 (69e680) 160 (87e340)

a-HCH 10 (1.0e70) 18 (1.3e110)

b-HCH 800 (100e3700) 1000 (200e3200)

g-HCH 0.45 (<0.1e2.2) 0.58 (<0.1e3.1)

HCHs 810 (100e3700) 1000 (210e3200)

p,p 0-DDE 600 (160e1700) 530 (140e1000)

p,p 0-DDD 2.2 (0.76e11) 3.6 (0.61e11)

p,p 0-DDT 50 (23e110) 52 (25e150)

DDTs 660 (190e1800) 580 (170e1100)

HCB 100 (23e430) 130 (23e880)

Oxychlordane 5.6 (0.87e13) 3.9 (1.3e7.4)

trans-Nonachlor 11 (<0.2e43) 5.3 (2.9e9.3)

cis-Nonachlor 2.1 (<0.2e7.1) 1.2 (0.46e4.5)

CHLs 19 (2.4e62) 10 (5.1e18)

TCPMe 1.1 (<0.2e3.8) 0.91 (<0.2e2.3)

PBDEsa 0.96 (0.46e1.7) NA

a PBDEs were analyzed in 10 samples obtained from primiparae with aver-

age age of 25 years (19e31 years).

use of the pesticide. On the other hand, CHL concentrationsdid not show any change and, taking into account the limiteduse of CHL in Russia (Fedorov and Yablokov, 1999), the levelsmight be considered as background.

Generally, HCHs and DDTs were detected at much higherconcentrations than the other OCs in human milk in the formerUSSR (Table 2). This seems to be a good illustration of long-standing intensive usage of the pesticides. According toFedorov and Yablokov (1999), DDT and HCH were themost widely used pesticides in the former USSR and wereproduced by several factories in the order of 1e5 and 0.1e1thousand tons per year, respectively (Zhulidov et al., 2002;Fedorov and Yablokov, 1999). The same authors presumethat even after official ban of agricultural use, the pesticidesmight have been applied in forestry, domestic or military uses.

When compared with other countries, HCH levels detectedin the present study were 1 to 2 orders of magnitude higherthan the corresponding levels in milk from Vietnam (Minhet al., 2004), Cambodia (Kunisue et al., 2004b), and Indonesia(Sudaryanto et al., 2006), but comparable with those in milkfrom China (Kunisue et al., 2004a) and India (Kunisueet al., 2002). Since China and India used the world’s largestamounts of HCH (Li, 1999), elevated HCH levels detectedin the present study, comparable to those in China and India,corroborate high human exposure to these contaminants inBuryatia. Among HCH isomers, b-HCH was the most abun-dant and contributed more than 95% to total HCHs (Table 1).Interestingly, the average value of a-HCH/b-HCH ratio(0.015) observed in the present study was higher than that inhuman milk from China (Kunisue et al., 2004a), the values be-ing 0.0034 and 0.0091 for Dalian and Shenyang, respectively.Relatively high proportion of a-HCH detected in the presentsamples may imply recent exposure to technical HCH. Whilecomparing with data for the 1990s, the HCH levels seemed tobe comparable with those in milk from Russian Arctic (Polderet al., 1998, 2003), Ukraine (Gladen et al., 1999), Mexico(Waliszewski et al., 1996), and Turkey (Cok et al., 1997),but one should bear in mind that the latter are not recent resultsand by now the levels might have changed.

DDT levels in the milk from Buryatia were generally lowerthan those in milk from developing countries where DDT, be-sides agricultural usage, was used also to control vector-bornediseases. However, the observed DDT levels were higher thanthe corresponding levels in milk from developed countriessuch as Sweden (Noren and Meironyte, 2000), Japan (Konishiet al., 2001), and England (Kalantzi et al., 2004).

Considering differences in the time of samplings, PCBlevels observed in this study were more or less comparablewith those detected in 1990s in milk from other Russianregions and former Soviet Republics (Table 2). The levelswere very similar to those in milk from developed countries(Japan, Sweden, and England) and one order of magnitudehigher than those found in milk from Asian developing coun-tries, including Cambodia, China, Vietnam, Malaysia, andIndonesia. High PCB levels observed in the present studymay reflect intensive past and current usage of PCBs inRussia. PCBs had been produced in Russia during 1939e1995

228 O.V. Tsydenova et al. / Environmental Pollution 146 (2007) 225e232

Table 2

Worldwide comparison of OC residues (ng/g lipid wt.) in breast milk samples from various countries

Country Year HCHs DDTs PCBs HCB CHLs TCPMe Reference

Former Soviet Union

Russia (Buryatia)b 2003e2004 810 660 240 100 19 1.1 This study

Russia (Irkutsk region)a 1988e1989 2100 2000 e 312 18 e Schecter et al., 1990

Russia (Barents region)a,b 1996e1997 320 1200 360 93 34 e Polder et al., 2003

Russia (Kola peninsula)a 1993 800 860 460 120 46 e Polder et al., 1998

Ukrainea 1993e1994 730 2800 590 170 38 e Gladen et al., 1999

Kazakstana 1994 2300 2300 380 91 e e Hooper et al., 1997

Other countries

Chinaa 1999e2000 1000 3200 38 e e e Wong et al., 2002

China (Dalian)b 2002 1400 2100 42 81 16 6.6 Kunisue et al., 2004a

China (Shenyang)b 2002 550 870 28 56 6.7 2.2 Kunisue et al., 2004a

Malaysiaa,b 2003 230 1600 80 11 23 8.1 Sudaryanto et al., 2005a

Vietnama,b 2000e2001 42 2700 82 3.5 5.2 5.5 Minh et al., 2004

Cambodiaa 1999e2000 5.2 1500 25 1.7 1.7 16 Kunisue et al., 2004b

Indonesiaa 2001e2003 16 1000 26 2 3.8 5 Sudaryanto et al., 2006

Indiaa 2000 720 430 70 1.3 5.5 e Kunisue et al., 2002

Mexicob 1994e1995 649 9473 e 30 e e Waliszewski et al., 1996

Turkeya 1995e1996 460 2400 e 50 e e Cok et al., 1997

Sweden 1997 e 140 320 12 e e Noren and Meironyte, 2000

Japanb 1998 210 290 200 14 85 e Konishi et al., 2001

England 2001e2003 40 220 200 20 e e Kalantzi et al., 2004

a Mean values of reported levels for more than one location.b Data from primiparous mothers only.

(Rosgidromet, 2000) and, according to an AMAP Report(Arctic Monitoring and Assessment Program (AMAP),2000), the production was stopped between 1990 and 1993.Although production of PCBs has ceased in Russia between1990 and 1993, PCB containing transformers and capacitorsare still in use. In 1999, in order to meet obligations ofStockholm Convention, the Russian Environment Conserva-tion Committee conducted an inventory of PCB containingequipment and wastes. About 200 thousand transformersand capacitors filled with totally about 18 thousand tons ofPCB containing oils were in use in 1999. Besides, at thetime of inventory there were about 1.5 thousand tons ofPCB containing wastes (Rosgidromet, 2000). It should benoted that currently in Russia there are no facilities forremoval or destruction of PCB/pesticide stockpiles that repre-sent a significant environmental problem.

As for HCB, it is noteworthy to mention that concentra-tions in the samples analyzed in this study and in milkfrom other places in Russia and former Soviet Republicswere the highest among the data published so far from differ-ent countries (Table 2). The HCB levels from the presentstudy were 1 to 2 orders of magnitude higher than the corre-sponding levels in milk from other countries. Although thereason for such high concentrations is still unclear, it maybe partially explained by the fact that 120e150 tons ofHCB were used annually for agricultural purposes until1991 (Fedorov and Yablokov, 1999). HCB is known tohave been used extensively in certain European countriesas a seed dressing fungicide (Kannan et al., 1992). Besides,HCB is still being used in Russia for production of pyrotech-nic and ordinance materials for the military (Speranskaya

et al., 2003). Generally, women in areas with less industrial-ization had significantly lower levels of HCB in their breastmilk (Solomon and Weiss, 2002). However, this is not sup-ported by the low HCB levels in Japanese and Swedishmilk samples included for the comparison. Schade andHeinzow (1998) reported that relatively high consumptionof meat (>700 g/week) was related to higher HCB levels.Since meat and dairy products were the main diet in Siberiahistorically, these eating habits might contribute to theobserved elevated concentrations of HCB. Other plausiblereason of elevated HCB levels is its atmospheric transportfrom lower latitude regions.

CHL concentrations observed in the study were comparableor slightly lower than those observed in milk from other loca-tions, except Japan (Table 2). The CHL levels in Japanese milksamples (Konishi et al., 2001) were higher than those observedin the present study. This could be expected because CHL waswidely used in Japan for termite control (Konishi et al., 2001).The purpose of CHL usage in Russia is not clear. Most prob-ably, it was used as a broad-spectrum insecticide (Fedorov andYablokov, 1999). Technical CHL mixture includes cis-chlor-dane, trans-chlordane, cis-nonachlor and trans-nonachlor.The epoxide metabolite oxychlordane is not a component ofthe original pesticide mixture; however, in almost all biologi-cal matrices it is the major component of CHLs (Dearth andHites, 1991). Oxychlordane and trans-nonachlor were pre-dominant compounds in breast milk samples analyzed in thisstudy (Table 1).

TCPMe concentrations were very low in the analyzed sam-ples. When compared with levels from other studies, in thepresent study the values were 1 to 2 orders of magnitude lower

229O.V. Tsydenova et al. / Environmental Pollution 146 (2007) 225e232

(Table 2). Low levels of TCPMe in the analyzed samplesimply lack of its sources in Buryatia.

All the above-mentioned data indicate that people in Bury-atia are exposed to relatively high levels of certain OCs suchas HCHs, PCBs and HCB. In this connection, it is very impor-tant to undertake further measures according to the StockholmConvention in order to reduce and eliminate PCBs and OCpesticides. Currently, in Russia there is an urgent need forappropriate technologies for destruction and disposal of bannedOC pesticide stockpiles and PCB containing equipment andwastes. Further studies are needed in order to identify reasonsfor high human exposure to the above-mentioned OCs andundertake measures towards its reduction.

3.1.2. PBDEsOut of the human milk samples analyzed for OCs, ten sam-

ples from primiparous mothers were also analyzed for PBDEs.All the milk samples showed detectable levels of PBDEs, al-though the levels were low and ranged from 0.46 to 1.7 ng/glipid wt. To understand magnitude of contamination byPBDEs, the results from this study were compared with thoseobserved for other countries (Table 3). Levels observed in thepresent study were 1 to 2 orders of magnitude lower than thosein milk from the United States (Schecter et al., 2003) andCanada (Gill et al., 2004), and comparable to correspondinglevels in milk from Asian developing countries, includingIndia, Vietnam, Indonesia, and Cambodia (Sudaryanto et al.,2005b). Magnitude of contamination by PBDEs in Buryatiaseems to be low, showing that humans are not undergoinghigh exposure to these contaminants. Unfortunately, there isno information about usage/production of brominated flame

retardants in Russia, and this adds uncertainty to the under-standing of PBDE sources and human exposure pathways.

Out of 14 congeners evaluated, BDE-28, BDE-47, BDE-100, BDE-153, BDE-197, and BDE-207 were detected in theanalyzed milk samples. Noteworthy is that BDE-209 concen-trations were below the detection limit (0.1 ng/g wet wt.),which was relatively high for this particular congener due to in-terference in blanks. The most common congeners detectedwere BDE-153, BDE-197, and BDE-207. In most of the studiesso far reported, octa- and nona-BDEs were not quantified (Lindet al., 2003; Schecter et al., 2003; Gill et al., 2004; Kalantziet al., 2004; Fangstrom et al., 2005). If only mono- to hepta-BDEs were considered, results of the present study are consistentwith published data, which suggest that BDE-153, BDE-100,BDE-47 are major congeners commonly found in human tissues(Gill et al., 2004). Among mono- to hepta-congeners, BDE-153was most abundant in this study, although BDE-47 usually dom-inates in human milk and tissues (Covaci et al., 2002; Guveniuset al., 2003; Schecter et al., 2003). Similarly, BDE-153 was themost abundant congener in milk samples from Faroe Islands(Fangstrom et al., 2005). Whereas abundance of BDE-47 inhuman tissues is usually explained by exposure to commercialpenta-BDE mixture (Petreas et al., 2003), which contains BDE-47 as one of the major components, prevalence of BDE-153may be a result of exposure to octa-BDE products (Gillet al., 2004). However, due to lack of information on PBDEusage in Russia it is quite difficult to interpret the presentresults and identify possible sources of PBDEs. Despite thelow levels of PBDEs in the analyzed human milk samples,future monitoring studies are needed as PBDE levels werefound to be exponentially increasing in most of the environ-mental compartments (Hites, 2004).

Table 3

Average levels (ng/g lipid wt.) of the most commonly detected congeners and total PBDEs in breast milk from various countries

Country Year n BDE-47 BDE-99 BDE-100 BDE-153 PBDEs Reference

Russia (Buryatia) 2003e2004 10 0.14 NDa 0.043 0.32 0.96 This study

North AmericaUSA 2002 47 40.8 14 8.2 5.3 73.9 Schecter et al., 2003

Canada 2001e2002 92 12.9 3.2 1.9 1.3 22.1 Gill et al., 2004

Europe

Faroe Island 1999 9 1.9 0.84 1 2.4 7.2 Fangstrom et al., 2005

UK 2001e2003 54 3 0.9 0.6 1.4 6.6 Kalantzi et al., 2004

Sweden 1996e1999 93 2.35 0.62 0.38 0.6 4.01 Lind et al., 2003

Asia

Japan 1998e2000 16 12.5 1.5 1.9 0.9 20 Akutsu et al., 2003

Japan 2000 13 1.5 0.38 0.41 1.2 3.8 Sudaryanto et al., 2005b

China 2004 19 0.49 0.12 0.15 0.74 6.2 Sudaryanto et al., 2005b

Malaysia 2003 5 1.6 0.42 0.32 0.65 3.5 Sudaryanto et al., 2005b

Korea 2004 9 0.81 0.2 0.34 0.79 2.6 Sudaryanto et al., 2005b

Philippines 2000 4 1.1 0.47 0.3 0.39 2.6 Sudaryanto et al., 2005b

Cambodia 2000 11 0.83 0.21 0.18 0.2 1.7 Sudaryanto et al., 2005b

Indonesia 2001e2003 30 0.39 0.18 0.15 0.32 1.3 Sudaryanto et al., 2005b

Vietnam 2000 10 0.11 0.1 0.08 0.32 1.1 Sudaryanto et al., 2005b

India 2000 5 0.27 0.11 0.06 0.1 0.6 Sudaryanto et al., 2005b

a Concentrations of BDE-99 in all the samples were lower than detection limit (DL ¼ 0.001 ng/g wet wt.).

230 O.V. Tsydenova et al. / Environmental Pollution 146 (2007) 225e232

3.2. OC levels and mother’s age/parity

Statistical analyses were performed in order to understandeffect of mother’s age and parity on OC levels in the milk sam-ples from Russia. Correlations between mother’s age and OClevels were examined separately for multiparous and primipa-rous mothers. In the case of primiparous mothers, concentra-tions of PCBs, HCB, CHLs and HCHs were significantlycorrelated with age (Fig. 2). This was consistent with theprevious reports as age is one of the most significant factorsaffecting OC residue levels in breast milk (Albers et al.,1996; Harris et al., 2001). Although DDT levels also tendedto increase with mother’s age in the same group, the correla-tion was not significant. In the case of multiparae, all theOC levels were not correlated with age.

It is well established that females excrete lipophilic con-taminants through gestation and lactation and, thus, pregnancyand consequent breastfeeding can lower levels of lipophiliccompounds in milk (Skaare and Polder, 1990; Waliszewskiet al., 1996; Schade and Heinzow, 1998; Harris et al., 2001;LaKind et al., 2004). In this study, when levels betweenprimiparae and multiparae were compared, DDT, PCB andCHL concentrations in the primiparae group appeared to behigher, but HCH and HCB levels were slightly higher in themultiparae group (Table 1). However, all the differenceswere not statistically significant. This may indicate the pres-ence of HCHs and HCB sources in the area and continuous

exposure of the women to these contaminants. Similarly,Waliszewski et al. (1996) found a decline of DDE and totalDDT levels with increasing parity but no such trend forHCH and HCB concentrations. Differences between OC con-centrations grouped by number of children were examined forunderstanding the possible effect of a number of previouspregnancies and consecutive lactations on OC levels. Al-though for most of the compounds levels appeared to decreasewith increasing parity, the differences between all the groupsfor all OCs were not significant (data not shown). This maybe due to the small sample number, late delivery of the secondchild and, hence, the long interval between deliveries leadingto uptake of OCs during the intervals.

3.3. Estimated daily intakes of OCs by infants

Daily intakes of OCs by infants were calculated based onthe assumption that the average milk consumption of a 5 kginfant is 700 g/day (Minh et al., 2004). The estimated daily in-take values were compared with tolerable daily intakes (TDIs)established by Health Canada (Table 4). The estimated intakesof HCHs for all samples (100%) were higher than the guide-line value. Estimated daily intakes of HCB, CHLs and PCBsfor 43%, 34% and 17% of samples, respectively, were higherthan the corresponding guideline values. Only for DDTs wereestimated daily intakes lower than the guideline limit.

Co

ncen

tratio

n (n

g/g

lip

id

w

t.)

0

100

200

300

400

500

R2 = 0.0965

p < 0.01

HCB

R2 = 0.5624

p < 0.01

0

20

40

60

80

15 20 25 30 35 40 45

CHLs

0

Age (years)

R2

= 0.3051

p < 0.01

0

200

400

600

800

PCBs

0

500

1000

1500

2000

DDTs

15 20 25 30 35 40 45

Trend in group

of primiparae

Primiparae

Multiparae

R2 = 0.2853

p < 0.05

1000

2000

3000

4000

HCHs

Fig. 2. Relationships between OC levels and mothers’ age.

231O.V. Tsydenova et al. / Environmental Pollution 146 (2007) 225e232

Table 4

Comparison of the estimated daily intakes of OCs (mg/kg body wt./day) with guideline values

PCBs HCHs HCB CHLs DDTs

TDIa 1 0.3 0.27 0.05 20

Estimated daily

intake (n ¼ 35)

0.77 3.2 0.54 0.06 2.3

(0.16e4.4) (0.38e25) (0.051e8.9) (0.0067e0.40) (0.61e10)

% of examinees

exceeding TDI

17 100 43 34 0

a Tolerable daily intake value proposed by Health Canada (cited from Oostdam et al., 1999).

However, in spite of the high percentage of breast milksamples with daily intake levels exceeding guideline values,it is unclear if the current concentrations of the OCs may causeany adverse effects. Even though persistent OCs are present inhuman milk, the benefits of breastfeeding are believed to out-weigh potential health risks from exposure to these chemicalsduring breastfeeding (LaKind et al., 2004). The advantages ofbreastfeeding for the mother and infant are numerous (Associ-ation of Women’s Health, Obstetric and Neonatal Nurses(AWHONN), 1999). Breastfeeding is particularly importantfor infants as it is indispensable in achieving optimal childhealth, growth, and development. Benefits to the mother in-clude reduced risk of developing osteoporosis, ovarian cancer,and postmenopausal breast cancer (American Academy ofPediatrics (AAP), 1997). Considering all these, the presenceof environmental chemicals in breast milk of women fromBuryatia should not discourage them from breastfeeding.

4. Conclusions

HCHs, DDTs, and PCBs were the most abundant contami-nants detected in the analyzed human milk samples, and thisseems to be a good illustration of historical intensive usageof HCH and DDT and ongoing usage of PCBs in Russia.

Comparison of the obtained data with results from otherregions indicates that people in Buryatia are exposed to rela-tively high levels of certain OCs, namely HCHs, PCBs, andHCB. This finding strengthens necessity for further activities,in addition to the official ban, toward reduction and elimina-tion of PCBs and OC pesticides in Russia and the need forfollow-up study to identify human exposure sources. In contrastto OCs, magnitude of contamination by PBDEs in the area islow and humans may not be undergoing high exposure to thesecontaminants presently.

The estimated daily intakes of HCHs, HCB, CHLs andPCBs by infants exceeded corresponding Health Canadaguidelines. However, the presence of environmental chemicalsin breast milk of women from Buryatia should not discouragethem from breastfeeding as breast milk is critically importantfor optimal child health, growth, and development.

Acknowledgments

The authors are grateful to Dr. A. Subramanian (CMES,Ehime University) for critical reading of the manuscript.This study was supported by Grants-in-Aid for Scientific

Research (A) (16201014) from the Japan Society for thePromotion of Science and Young Scientists (B) (Project16780139) and ‘‘21st century COE program’’ from the Minis-try of Education, Culture, Sports, Science and Technology,Japan, and ‘‘Materials Cycles Modeling of Persistent ToxicChemicals and its policy Research Applications for Recyclingand Waste Management’’ from the Waste ManagementResearch Grants of the Ministry of the Environment, Japan.A Joint Japan/World Bank Graduate scholarship awarded toO.V.T. is gratefully acknowledged.

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