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                    Pediatric Lead Exposure From Imported Indian Spices and Cultural
                                             Powders

                                                Cristiane Gurgel Lin, MD, PhD,




                    Embargo Release Date: Monday, March 15, 2010 - 12:01am (ET)




                                                      Embargo Policy:
                                    Information in this article is embargoed for release until the
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              The American Academy of Pediatrics, 141 Northwest Point Blvd., Elk Grove Village, IL 60007
Pediatric Lead Exposure From Imported Indian Spices
and Cultural Powders
       WHAT’S KNOWN ON THIS SUBJECT: Lead is a neurotoxin, and               AUTHORS: Cristiane Gurgel Lin, MD, PhD,a,b,c Laurel Anne
       elevated BLLs in children are a public health concern. Immigrant      Schaider, PhD,d Daniel Joseph Brabander, PhD,e and Alan
       children are at risk because of additional exposure to imported       David Woolf, MD, MPHb,f
                                                                             a
       culture-specific leaded products. Lead contamination in many            Pediatric Residency Program, Department of Medicine, and
                                                                             fPediatric Environmental Health Center, Division of General
       imported products has not been characterized.
                                                                             Pediatrics, Children’s Hospital Boston, Boston, Massachusetts;
                                                                             bDepartment of Pediatrics, Harvard Medical School, Boston,
       WHAT THIS STUDY ADDS: We report here lead-poisoning cases             Massachusetts; cDepartment of Neonatology, Pediatrix Medical
       from Indian cultural powders or spices. Imported products             Group, Seton Medical Center, Austin, Texas; dDepartment of
       surveyed contained lead, and chronic exposure could increase          Environmental Health, Harvard School of Public Health, Boston,
       the prevalence of elevated BLLs. These results increase leaded-       Massachusetts; and eDepartment of Geosciences, Wellesley
                                                                             College, Wellesley, Massachusetts
       product awareness and aid lead-poisoning prevention.
                                                                             KEY WORDS
                                                                             pediatric lead poisoning, childhood plumbism, spices, herbal
                                                                             products, cosmetics, religious powders, lead contamination,
                                                                             Indian, sindoor, culture-specific exposure

abstract                                                                     ABBREVIATIONS
                                                                             CDC—Centers for Disease Control and Prevention
                                                                             BLL— blood lead level
BACKGROUND: Significant lead poisoning has been associated with
                                                                             FDA—Food and Drug Administration
imported nonpaint products.                                                  IEUBK—integrated exposure uptake biokinetic model for lead in
OBJECTIVES: To describe cases of pediatric lead intoxication from im-        children
                                                                             PEHC—Pediatric Environmental Health Center
ported Indian spices and cultural powders, determine lead concentra-         XRF—x-ray fluorescence
tions in these products, and predict effects of ingestion on pediatric       NIST—National Institute of Standards and Technology
blood lead levels (BLLs).                                                    LOD—limit of detection
                                                                             SBET—simple bioaccessibility extraction test
PATIENTS AND METHODS: Cases and case-study information were ob-              XRD—x-ray diffraction
tained from patients followed by the Pediatric Environmental Health          ZPP—zinc-chelated protoporphyrin
                                                                             CI— confidence interval
Center (Children’s Hospital Boston). Imported spices (n          86) and
cultural powders (n 71) were analyzed for lead by using x-ray fluo-           www.pediatrics.org/cgi/doi/10.1542/peds.2009-1396

rescence spectroscopy. The simple bioaccessibility extraction test was       doi:10.1542/peds.2009-1396
used to estimate oral bioavailability. The integrated exposure uptake bio-   Accepted for publication Nov 16, 2009
kinetic model for lead in children was used to predict population-wide       Address correspondence to Cristiane Gurgel Lin, MD, PhD,
geometric mean BLLs and the probability of elevated BLLs ( 10 g/dL).         Neonatology Department, Seton Medical Center, 1201 W 38th St,
                                                                             Austin, TX 78705. E-mail: cristiane.lin@gmail.com
RESULTS: Four cases of pediatric lead poisoning from Indian spices or        PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275).
cultural powders are described. Twenty-two of 86 spices and foodstuff
                                                                             Copyright © 2010 by the American Academy of Pediatrics
products contained 1 g/g lead (for these 22 samples, mean: 2.6 g/g
                                                                             FINANCIAL DISCLOSURE: The authors have indicated they have
[95% confidence interval: 1.9 –3.3]; maximum: 7.6 g/g). Forty-six of 71       no financial relationships relevant to this article to disclose.
cultural products contained 1 g/g lead (for 43 of these samples, mean:
8.0 g/g [95% confidence interval: 5.2–10.8]; maximum: 41.4 g/g). Three
sindoor products contained 47% lead. With a fixed ingestion of 5 g/day
and 50% bioavailability, predicted geometric mean BLLs for children aged
0 to 4 years increased from 3.2 to 4.1 g/dL, and predicted prevalence of
children with a BLL of 10 g/dL increased more than threefold (0.8%–2.8%).
CONCLUSIONS: Chronic exposure to spices and cultural powders may
cause elevated BLLs. A majority of cultural products contained 1
  g/g lead, and some sindoor contained extremely high bioaccessible
lead levels. Clinicians should routinely screen for exposure to these
products. Pediatrics 2010;125:e828–e835


e828    LIN et al
ARTICLES


Lead is a neurotoxin that can cause           assess lead contamination among var-        (2) religious powders (used in reli-
permanent neurocognitive deficits in           ious commercially available imported        gious or cultural practices, not in-
children.1–3 The current Centers for          Indian spices and ceremonial prod-          tended for consumption, not labeled
Disease Control and Prevention (CDC)          ucts sold in stores in the Boston, Mas-     for use as medication). When more
blood lead level (BLL) of concern is 10       sachusetts, area, and (3) predict the       than 1 store carried the same brand of
  g/dL, although a BLL of 5 g/dL              prevalence of elevated BLLs in children     a given product, it was only purchased
also may result in cognitive deficits.4–8      caused by chronic exposure to these         once. The name, manufacturer, manu-
A national objective of Healthy People        products by using the integrated expo-      facturer’s location, packaging loca-
2010 is to eliminate elevated BLLs in         sure uptake biokinetic model for lead       tion, lot number, expiration date, store
children. As part of this effort, the CDC     in children (IEUBK).23                      name, and purchase date were re-
has worked to identify at-risk popula-                                                    corded when available. For compari-
tions and nonpaint sources of lead ex-        PATIENTS AND METHODS                        son, 10 types of spices produced by US
posure.3,9 Among those at risk are im-        Case-Study Information                      manufacturers were purchased at a
migrant children, who are more likely                                                     large New England supermarket, al-
                                              Case-study information was acquired         though in most cases, the country of
than US-born children to have an ele-
                                              through the review of medical charts        origin was not listed.
vated BLL through exposure to non-
                                              of patients who were referred to the
paint lead sources.10,11 Culture-specific                                                  To assess variability between lots of
                                              Pediatric Environmental Health Center
nonpaint lead sources have been iden-                                                     the same product, all products that
                                              (PEHC) at Children’s Hospital Boston
tified, including imported utensils,12                                                     contained 10 g/g lead were repur-
                                              from 2006 to 2008 for an elevated BLL.
foods such as Mexican tamarind                                                            chased for additional analysis. In addi-
                                              The cases represent 2% of new pa-
candy,13 cosmetics such as kohl14 and                                                     tion, 10% of the spices and powders
                                              tient referrals to the PEHC. All patients
henna,15 and ayurvedic traditional                                                        were randomly selected for repur-
                                              were asymptomatic. Home environ-
medicines16,17 and Mexican digestive                                                      chase and reanalysis.
                                              ments were assessed for lead by the
remedies.18
                                              Massachusetts Department of Public
Culture-specific lead sources have                                                         Heavy-Metal Analysis
                                              Health via dust wipe and direct sam-
placed South Asian and Indian commu-          pling of surfaces and by the PEHC via       Samples were labeled with a numeri-
nities at risk. Woolf and Woolf19 re-         environmental inventory and soil-           cal identifier only. Four grams of each
ported 2 cases of pediatric lead poi-         testing. In all cases, no other signifi-     sample were transferred into x-ray flu-
soning from imported Indian spices. In        cant sources of lead were found.            orescence (XRF) analytical cups (Pre-
addition, a Thai infant suffered lead                                                     mier Lab Supply, Port St Lucie, FL) with
poisoning from a powder applied to his        Collection Methods: Market-Basket           4- m windows (Spex Certiprep,
tongue,20 and an Indian child devel-          Survey                                      Metuchen, NJ) after thorough homog-
oped an elevated BLL from ingestion of        In this article, we use the terms “cul-     enization. Repurchased products re-
sindoor (a powder applied to a wom-           tural powder,” “religious powder,” and      ceived new numerical identifiers, and
an’s scalp as a marriage sign).21 Re-         “ceremonial powder” interchangeably.        2 aliquots of each repurchased prod-
cently, the US Food and Drug Adminis-         Collection and analysis of spices and       uct were analyzed.
tration (FDA) recalled a brand of             powders were based on the protocol          The concentration of lead in each sam-
ceremonial Indian powders because of          outlined by Saper et al.16 Boston-area      ple was determined by using a Spectro
lead contamination and confirmed               stores that sell spices and religious       XEPOS polarized energy-dispersive XRF
cases of lead poisoning.22                    powders were identified through an           instrument (Spectro Analytical, Kleve,
To date, few studies have systemati-          online national directory of Indian gro-    Germany). Measurement accuracy
cally investigated the lead content of        cery stores24 and a New England area        was determined by using a standard
imported Indian spices and ceremo-            Indian community business directo-          reference material (National Institute
nial powders and considered related           ry.25 In early 2008, 15 randomly se-        of Standards and Technology [NIST]
risks posed to children living in the         lected stores were visited within 20        2709, San Joaquin [California] soil).26
United States. The goals of our investi-      miles of Children’s Hospital Boston.        The measured mean lead concentra-
gation were to (1) describe recent            Spices and ceremonial powders were          tion for NIST 2709 (18.5 0.9 g/g; n
cases of pediatric lead poisoning             purchased if they were manufactured         48) was consistent with the certified
caused by contaminated Indian spices          in India and were (1) spices/foodstuffs     value (18.9      0.5 g/g). The limit of
and religious powders, (2) survey and         (edible, used in food preparation) or       detection (LOD) is 1.0 g/g.


PEDIATRICS Volume 125, Number 4, April 2010                                                                                  e829
Because many spice samples were be-          IEUBK Modeling                               hemoglobin level of 11.2 g/dL, and
low the XRF LOD, total lead concentra-       The IEUBK model, Windows version 1.0,        hematocrit level of 31.7%. He received
tion was also determined in a subset of      build 264 (US Environmental Protec-          5 days of parenteral chelation with
spices by using microwave digestion in       tion Agency, Washington, DC), is a nu-       intravenous Na2CaEDTA. His zinc-
concentrated nitric acid followed by in-     merical blood lead predictive mod-           chelated protoporphyrin (ZPP) level
ductively coupled plasma mass spec-          el.23,31 The IEUBK model estimates           was elevated at 152 mol/mol of heme
trometry (Elan 6100 [Perkin Elmer,           population-level BLLs on the basis of        (normal ZPP level, based on a hemato-
Shelton, CT]) analysis. The LOD is           various lead-exposure sources, uptake        crit level of 35%: 25– 65 mol/mol),
   0.03 g/g. Average recovery of lead        via inhalation or ingestion, and bioki-      which suggested chronic lead expo-
from NIST 1515 (apple leaves) was 88%        netics. Probability distributions are        sure. The parents described rubbing a
(n 2).                                       used to estimate variability in BLLs         religious powder on the patient’s fore-
                                             among exposed children.23 The IEUBK          head since he was several weeks old.
Bioaccessibility Analysis                                                                 They did not add powders to foods.
                                             model has been widely used since 1994
For a random subset of samples, lead                                                      Lead analyses revealed 89 000 g/g
                                             and independently validated and veri-
bioaccessibility (ie, fraction of metal                                                   lead in the religious powder and 300
                                             fied.32 Because it has been used to es-
mobilized in a biologically relevant                                                        g/g lead in an eye cosmetic. The par-
                                             timate mean BLLs and predict the
fluid) was estimated by using the sim-                                                     ents stopped using the powder, and
                                             probability of elevated BLLs in a popu-
                                                                                          the child received oral chelation with
ple bioaccessibility extraction test         lation of children exposed to lead-
                                                                                          dimercaptosuccinic acid for 6 months,
(SBET). The SBET is an in vitro gastric      contaminated tamarind candy,33 the
                                                                                          which reduced the BLL to 21 g/dL.
fluid extraction that simulates metal         model was considered appropriate for
                                                                                          By 21 months of age, the child’s BLL
dissolution in the stomach and has           the goals, age ranges, and exposure du-
                                                                                          was stable (15 g/dL), and he required
been shown to predict in vivo lead ab-       ration for our population of concern.
                                                                                          no additional oral chelation therapy.
sorption in juvenile swine, a model for      We used the IEUBK model to estimate
gastrointestinal absorption in chil-         the geometric mean BLL for a popula-         Case 2
dren.27,28 The SBET was performed by         tion and to predict the probability of       A 9-month-old Indian boy was referred
following a previously published proto-      elevated BLLs caused by intentional          for an elevated BLL (21 g/dL). The par-
col.29 Bioaccessibility was calculated       or accidental ingestion of lead-             ents described applying an orange
as extracted lead concentration/total        contaminated spices or powders. Lead         powder (orange shringar) to his fore-
lead concentration.                          exposure from other environmental            head as a religious tradition. They did
To determine the crystalline phases          sources was held constant, and stan-         not add powders to food. Lead analy-
linked with high-lead sindoor products       dard model inputs, comparable to Bos-        ses revealed 220 000 g/g in the pow-
( 47% lead), x-ray diffraction (XRD)         ton background levels,26,34,35 were used     der and 49 g/g in both holy ash and
analyses were conducted by using a           to incorporate background lead expo-         kumkum. Analyses of family spices and
rotating copper anode RU 300 genera-         sure. Diet inputs were calculated from       utensils did not detect lead. The par-
tor (Rigaku, Tokyo, Japan). Resulting        FDA food-monitoring data.36 For model        ents stopped using the powders, and 4
XRD patterns were fit by using Jade           runs, an alternate exposure function         weeks later the patient’s BLL was 17
software (Materials Data, Livermore,         was used to model additional ingestion         g/dL, with a ZPP level of 85 mol/mol
CA) with search/match of the FIZ-            of spices or powders. Bioaccessibility,      and hemoglobin level of 10.7 g/dL. Two
Inorganic Crystal Structure Database         based on SBET data, was used as an           months later, his BLL decreased to 13
(http://icsd.ill.eu/icsd/index.html) and     upper-bound estimate of bioavailability        g/dL. No chelation was administered.
Rietveld whole-pattern fitting. XRD           (ie, fraction of lead that is absorbed and
analyses provide both phase identifi-         reaches the systemic circulation).28,37      Case 3
cation and the general bonding envi-                                                      A 3-year, 9-month-old Indian girl was
ronment of lead. Combining XRD char-         RESULTS                                      referred for an elevated BLL (18 g/
acterization with SBET analysis is an        Case Summaries                               dL), a ZPP level of 88 mol/mol, and a
effective and underutilized approach                                                      hemoglobin level of 10.9 g/dL. No con-
to evaluating the chemical form and          Case 1                                       taminated herbs, spices, or ethnic
relative solubility of lead in various ex-   A 10-month-old Indian boy was re-            remedies were discovered. However, a
posure media (soils, spices, religious       ferred for an elevated BLL (43 g/dL), a      religious powder ingested regularly by
powders).30                                  mean corpuscular volume of 69.7 fL,          the patient contained 4800 g/g lead.


e830    LIN et al
ARTICLES


TABLE 1 Examples of Cosmetics, Hair Products, and Ceremonial Powders Purchased                                         tistical analysis (Table 3). These sin-
       Product Name                                Brand Name                                    Uses                  door lead concentrations are compa-
Cosmetics and hair products                                                                                            rable to those in published reports.21,38
  Aritha powder                     Hesh                                                Shampoo                        Cosmetics and ceremonial powders
  Henna                             Al-aroosa, Ancient Secret, Ayur, Dulhan             Hand decoration
  Kajal                             Shingar Ltd, Western Indian Chemical Co             Eyeliner                       had similar lead concentration and
  Hairwash                          Meera                                               Shampoo                        ranges (Table 3).
  Sandalwood                        Nirav                                               Cosmetic, medicinal
Ceremonial powders
  Abil                              Bhavani, Nirav                                      Pooja ceremony
                                                                                                                       Indian Spices and Foodstuff
  Gulal                             MDHD, Swad, Durbar                                  Pooja ceremony                 Eighty-six food products manufac-
  Kumkum                            Shringar, Topaz, Butala Emporium                    Bindi
  Sindoor                           MDHD, Swad, Nirav, Butala Emporium                  Marriage symbol
                                                                                                                       tured by 53 companies were pur-
                                                                                                                       chased (Table 2). Sixty-three prod-
                                                                                                                       ucts listed packaging location, and 38
The family discontinued use of this                   seed (0.6 g/g), asafoetida (0.8 g/g),                            products listed lot numbers. Thirty-
powder, and over the next 8 months,                   and turmeric (1.4 g/g). The family                               eight products were categorized as
the patient’s BLL decreased to 8 g/dL.                discontinued use of all imported                                 common spices, used daily in food
                                                      spices, and the patient’s BLL declined                           preparation, whereas 48 were catego-
Case 4                                                to 14 g/dL within 6 months.                                      rized as foodstuff, including spice
A 12-month-old Indian boy was re-                                                                                      mixes, food coloring, or other food ad-
ferred for an elevated BLL (28 g/dL), a               Religious Powders                                                ditives, which may be used less fre-
ZPP level of 103 mol/mol, and a hemo-                 Seventy-one religious products manu-                             quently. Of the 86 products tested by
globin level of 9 g/dL. Analyses of                   factured by 28 companies were pur-                               XRF, 22 (26%) contained 1 g/g lead,
spices, herbal remedies, and religious                chased (Table 1). Forty-three products                           with a mean lead concentration in
powders revealed that several Indian                  listed packaging location, and 5 prod-                           these 22 samples of 2.6 g/g (95% CI:
spices, used daily, contained lead: an                ucts provided lot numbers. Sixteen                               1.9 –3.3) and a maximum of 7.6 g/g
herb mix (11 g/g), brown mustard                      products were categorized as cosmet-                             (sea salt). Food products had a lower
                                                      ics and hair products for daily use, and                         percentage of samples with detected
                                                      55 were categorized as ceremonial re-                            lead and lower mean lead concentra-
TABLE 2 Examples of Spices and Foodstuff
          Purchased                                   ligious powders for daily to monthly                             tion compared with religious prod-
  Product Name                Brand Name              use.                                                             ucts. Spices and foodstuff contained
Spices                                                Of the 71 cultural products tested, 46                           similar ranges of lead concentration
  Black pepper        Laxmi, Swad, Deep               (65%) contained 1 g/g lead. The                                  (Table 3).
  Cardamom            DEEP
  Chili powder        Saras, Noer, Swan               mean lead concentration in 43 sam-                               On the basis of a direct comparison of
  Coriander           MDHD, Periyar, Swad, Swan       ples with detectable lead (excluding 3                           10 types of spices (US brands and im-
  Fennel powder       Deep                            high-lead sindoor products) was 8.0                              ported) analyzed by inductively cou-
  Fenugreek           Swad
                                                        g/g (95% confidence interval [CI]:                              pled plasma mass spectrometry, im-
  Garam masala        MDHD, Swan
  Garlic power        Shalimar                        5.2–10.8 g/g), with a maximum of                                 ported spices had a mean lead
  Ginger powder       Himgiri, Swad                   41.4 g/g (kajal). Three sindoor prod-                            concentration of 0.5 g/g (95% CI:
  Paprika             Swad                                                                                             0.18 – 0.72), which was twice the mean
                                                      ucts contained 47% lead by weight
  Sindav salt         Deep, Swad
  Turmeric            Laxmi, Nirav, Swad, Swan        and were treated separately in the sta-                          lead concentration of US-brand spices
Foodstuff
  Food coloring       Bush, Bhavani, Narmada,
                        Vesco                         TABLE 3 Mean Concentration, CI, and Range of Lead in Spices, Foodstuff, Cosmetics, Ceremonial
  Dabelli masala      Bombay Magic                                Powders, and High-Lead Sindoor With a Detectable Lead Level by XRF
  Fish curry          MDH                                    Product               No. of          Samples With                  Lead Level, Mean               Range, g/ga
  Vada mix            MTD                                                         Samples        Detectable Lead, %               (95% CI), g/ga
  Chappli kabab       Roopak                          Spices                          38                   24                    2.6 (1.2–4.0)                      1–7.6
     masala                                           Foodstuff                       48                   27                    2.6 (1.8–3.4)                      1–6.3
  Vermacelli mix      MTR                             Cosmetics                       16                   81                    7.6 (1.3–13.9)                     1–41.4
  Tulsi powder        Bhavani                         Ceremonial powders              52                   58                    8.2 (6.0–10.4)                     1–39.9
  Karela powder       Swad                            High-lead sindoor                3                  100              559 000 (463 000–655 000)          469 000–638 000
  Asafoetida          Laljee Godhoo, Ruchi, Swad      a Serial dilutions of NIST 2709 suggest that the LOD (based on the criteria that samples run in triplicate maintain     10%
  Amchur powder       Deep
                                                      relative SD) is 1.0 g/g (data not shown). LOD estimates based on serial dilution of NIST 2709 were supported by 15 replicate
  Hajmola candy       Dabur India Ltd                 analyses of NIST 1515 (apple leaves) in which a 20% SD was observed for an expected lead concentration of 0.47 g/g.



PEDIATRICS Volume 125, Number 4, April 2010                                                                                                                                 e831
(0.19 g/g [95% CI: 0.1– 0.28]) (Table                        form of lead in these samples. Minium                             for children aged 0 to 4 years in-
4). However, this difference was not                         is commonly used as a pigment in                                  creased from 3.2 to 4.1 g/dL, and the
significant on the basis of a pairwise t                      henna and lead paint.15,43                                        predicted prevalence of children with
test (P .1). The lead concentration in                                                                                         an elevated BLL increased threefold,
these 10 imported spices was up to                           IEUBK Modeling                                                    from 0.8% to 2.8%. The difference is
fivefold higher than the recommended                          The IEUBK model was used to predict                               more dramatic with small increases in
maximum level in hard candy (0.1 g/                          the effects of chronic ingestion of                               ingested amount and bioavailability
g).39 In addition, imported spices had a                     spices or religious powders on popula-                            (Figs 1 and 2); at 5 g/day and 80%
similar range of lead concentrations                         tion BLLs. For a fixed ingestion rate                              bioavailability, 4.9% of children were
as spices manufactured in Pakistan                           ( g/day), the geometric mean BLL and                              predicted to have an elevated BLL, and
(0.02–9.2 g/g).40 Although the FDA has                       percentage of children with an ele-                               at 10 g/day and 50% bioavailability,
no recommended maximum lead con-                             vated BLL (defined as a BLL of 10 g/                               6.5% of children were predicted to
centration for spices, the European                          dL) were calculated. When the model                               have an elevated BLL. These results
Union’s recommended limit for dried                          was run with default inputs only, the                             suggest that infants and children can
herbs is 2 to 3 g/g.41                                       background geometric mean BLL for                                 develop lead poisoning by chronic in-
                                                             children aged 1 to 5 years was 3.1 g/                             gestion of contaminated spices and
Bioaccessibility                                             dL. This value is higher than the na-                             ceremonial powders.
We determined bioaccessibility for a                         tional geometric mean BLL of 1.9 g/dL
subset of samples by SBET as a reason-                       but comparable to that of black chil-                             DISCUSSION
able approximation for bioavailabil-                         dren (2.8 g/dL) and children in low-                              Our analyses demonstrate the risk of
ity.28 Spices had a mean lead bioacces-                      income households (2.5 g/dL).44 The                               lead poisoning associated with con-
sibility of 49% (95% CI: 32– 66) (Table                      percentage of children with an ele-                               taminated ceremonial powders and
5), which is consistent with previously                      vated BLL (0.6%) was lower than the                               rituals that involve the external appli-
published data37,42 and with the default                     national average (1.6%).44 Overall, these                         cation of these powders to young in-
IEUBK value of 50% for lead absorption                       data suggest that the model can reason-                           fants. Of particular concern are (1) the
from food.37 Religious and cosmetic                          ably approximate background BLL for                               extremely high lead concentrations
products and sindoor (with 47%                               children who live in the United States.                           found in some readily available sin-
lead) had similar mean lead bioacces-                        To model increased exposure resulting                             door powders (47%– 64% lead), (2) the
sibility (50%–56%) as spices (Table 5).                      from spice or accidental powder inges-                            moderate lead concentrations found
XRD results indicated that Pb3O4                             tion, we used a fixed lead-ingestion rate                          in other cultural powders (up to 40 g/
(minium, “red lead”) is the chemical                         (5 g/day). Spice-ingestion rates for                              g), (3) the young age at which parents
                                                             various lead concentrations are listed                            commence such practices, and (4) the
TABLE 4 Mean Concentration, CI, and Range                    in Table 6 and are comparable to those                            chronic nature of the exposure (up to
             of Lead in US-Brand Spices and                  in published reports.45,46 When the                               several times per week). Although the
             Indian Brand Spices (N 10)
                                                             model was run with a fixed ingestion                               powders are not meant for consump-
  Producta             Lead Level, Mean          Range,
                        (95% CI), g/g              g/g       rate of 5 g/day and 50% bioavailabil-                             tion, we speculate that infants may be
US brands              0.19 (0.1–0.28)          0.03–0.41    ity, the predicted geometric mean BLL                             inadvertently exposed by hand-to-
Indian brands          0.45 (0.17–0.73)         0.12–1.54                                                                      mouth transference of topically ap-
a Spices tested included garlic powder, black pepper, fen-                                                                     plied powders or by the hands of par-
nel powder, ginger powder, coriander, garam masala, tur-                                                                       ents who handle the powder and then
                                                             TABLE 6 Ingestion Rate as a Function of Lead
meric, chili powder, paprika, and cardamom.
                                                                          Concentration for Lead Ingestion of                  prepare foods for the infant’s con-
                                                                          5 g/g
                                                                                                                               sumption. Infants may also be exposed
                                                                 Lead             Daily Ingestion            Weekly
TABLE 5 Mean Bioaccessibility, CI, and Range                                                                                   to these products in utero, through
             of Bioaccessibility of Religious                Concentration,            Ratea             Ingestion Rate
             Powders, Spices, and High Lead                       g/g             g     Teaspoons        g     Teaspoons
                                                                                                                               breastfeeding, inhalation of aerosol-
             Sindoor                                                                                                           ized particles, or dermal absorption.12
                                                                    0.5         10          2          70         14
 Product        No. of           Mean             Range,            1            5          1          35          7           As predicted by IEUBK modeling,
               Samples      Bioaccessibility,       %               5            1          0.2         7          1.4
                                                                   10            0.5        0.1         3.5        0.7
                                                                                                                               chronic exposure can have a dramatic
                               % (95% CI)
                                                                   20            0.25       0.05        1.75       0.35        effect on BLL. For instance, ingesting
Powders            6           56 (20–92)         20–80
Spices            10           49 (32–66)         22–100
                                                             a Mean ingestion rate of spices in g/day for children aged        20 g of high-lead sindoor increases
                                                             1 to 3 years, living in India, was reported to be 5 g/day, with
High-lead          3           50 (38–62)         40–62
                                                             a range of 3 to 10 g/day, as reported by the National Nutri-
                                                                                                                               lead exposure by 10 g/day and the
   sindoor                                                   tion Monitoring Bureau.45,46                                      probability of elevated BLL by eightfold.


e832       LIN et al
ARTICLES


                                                                                                          ated. Such items include cosmetics,
                                                                                                          such as kohl,14 and we now extend
                                                                                                          the product list to include Indian
                                                                                                          powders intended for use in reli-
                                                                                                          gious practices.
                                                                                                          We also found that under certain cir-
                                                                                                          cumstances, exposure to imported In-
                                                                                                          dian spices may increase the preva-
                                                                                                          lence of elevated BLL. IEUBK modeling
                                                                                                          predicted that chronic ingestion of
                                                                                                          spices that contained our highest mea-
                                                                                                          sured lead concentration (7.6 g/g)
                                                                                                          may result in elevated BLLs. Therefore,
                                                                                                          a risk for lead poisoning exists if there
                                                                                                          is sufficient lead contamination or a
                                                                                                          high daily dose. This risk is not theoret-
                                                                                                          ical, as indicated by our case report of
                                                                                                          lead poisoning from chronic ingestion
                                                                                                          of imported spices with similar lead
FIGURE 1                                                                                                  concentrations (1–11 g/g).
The IEUBK model was used to predict mean geometric BLLs in children aged 0 to 4 years with varying
exposures. In this simulation, daily lead ingestion and bioavailability were varied, and resulting BLLs   There are several limitations of our
are shown.                                                                                                study. First, although we analyzed
                                                                                                          more than 150 products, our samples
                                                                                                          did not represent all types of Indian-
                                                                                                          manufactured products. Second, there
                                                                                                          may be lot-to-lot variability in lead
                                                                                                          concentration depending on manu-
                                                                                                          facturing and packaging practices
                                                                                                          and on natural spice-plant accumu-
                                                                                                          lation of lead. Third, regional varia-
                                                                                                          tion in Indian product availability and
                                                                                                          distribution may limit the applicabil-
                                                                                                          ity of the study to other locations.
                                                                                                          Fourth, family usage patterns will af-
                                                                                                          fect the overall cumulative exposure
                                                                                                          and risk of injury. We did not acquire
                                                                                                          end-user information regarding
                                                                                                          these products. Nevertheless, to our
                                                                                                          knowledge, our study represents the
FIGURE 2                                                                                                  first attempt to investigate a variety
The IEUBK model was used to predict the prevalence of BLLs of 10 g/dL in a population of children         of cultural products and to carefully
aged 0 to 4 years with varying exposures. In this simulation, daily lead ingestion and bioavailability
were varied.
                                                                                                          consider their potential effects on
                                                                                                          pediatric BLL.

Ingestion of 250 mg of sandalwood, an                 studies have shown risks to children                CONCLUSIONS
amount comparable to pediatric soil                   from remedies, foods, and spices                    Our investigation of Boston-area
ingestion through hand-to-mouth ac-                   meant for consumption,16–19,48 lead                 stores that sell Indian spices and reli-
tivities,47 increases exposure by 5 g/                poisoning from contaminated prod-                   gious powders revealed a ready avail-
day and the probability of elevated                   ucts intended only for external appli-              ability of lead-contaminated items.
BLL by threefold. Although previous                   cation has not been fully appreci-                  Similar products can also be pur-


PEDIATRICS Volume 125, Number 4, April 2010                                                                                                    e833
chased on the Internet. Furthermore,                itored, and low-lead sindoor ( 5                      pretation of the data; or preparation,
we were able to purchase highly con-                  g/g) could be suggested as a safer                  review, or approval of the manu-
taminated items that were previously                alternative. Closer inspection and                    script for submission.
banned or recalled by the FDA. The high             testing of other religious products is                Ms Suzanne Giroux (PEHC, Children’s
prevalence, availability, chronic and               warranted.                                            Hospital Boston) assisted in ascertain-
widespread use,49 and potential toxic-                                                                    ing the clinic families identified for in-
                                                    ACKNOWLEDGMENTS
ity of these products pose a public                                                                       clusion in the case series. James Be-
                                                    Dr Lin was supported by the Lovejoy
health risk. Clinicians should be aware                                                                   sancon, PhD (associate professor of
                                                    Residency Research Fund (Children’s
of these and other imported hazards                 Hospital Boston). Dr Woolf was sup-                   geosciences at Wellesley College) con-
and inquire about their use during rou-             ported in part by a grant from the                    ducted the XRD analyses on the sin-
tine health supervision visits. Further-            Agency for Toxic Substances and Dis-                  door samples. Ms Emily Estes, Ms
more, per CDC and American Academy                  ease Registry Superfund Reconcilia-                   Nooreen Meghani, and Ms Megan
of Pediatrics recommendations, clini-               tion and Reclamation Act, adminis-                    Carter-Thomas (Wellesley College) as-
cians who work with South Asian com-                tered through the Association of                      sisted with XRF sample analysis and
munities should perform targeted BLL                Occupational and Environmental Clin-                  assessment of standards performance.
screening on new immigrants and rou-                ics Association (Washington, DC). Chil-               Ami Zota, ScD (Program on Repro-
tinely administer lead-exposure risk-               dren’s Hospital Boston, Harvard Medi-                 ductive Health and the Environment,
assessment questionnaires (provided                 cal School, Harvard School of Public                  University of California, San Fran-
by state departments of health50,51),               Health, Wellesley College, Stanford Uni-              cisco, CA) and Ananya Roy, ScD (De-
modified to include these hazards.52,53              versity School of Medicine (Dr Lin’s                  partment of Health Sciences, School
Because of the high lead concentra-                 former affiliation), and Pediatrix                     of Public Health, University of Michi-
tions found in some sindoor sam-                    Medical Group had no role in the de-                  gan, Ann Arbor, MI) reviewed earlier
ples, import, sale, and labeling of                 sign or conduct of the study; collec-                 drafts of this manuscript. None re-
these items should be carefully mon-                tion, management, analysis, or inter-                 ceived compensation.
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PEDIATRICS Volume 125, Number 4, April 2010                                                                                                                  e835

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Dangerous Indian Spices

  • 1. Page 1 of 9 Pediatric Lead Exposure From Imported Indian Spices and Cultural Powders Cristiane Gurgel Lin, MD, PhD, Embargo Release Date: Monday, March 15, 2010 - 12:01am (ET) Embargo Policy: Information in this article is embargoed for release until the date indicated above. Interviews may be conducted prior to the embargo release date, but nothing may be aired or published. If you are a media representative and have questions about the embargo, upcoming press events, or other matters, please contact AAP Communications staff at 847-434-7877, or via e-mail at commun@aap.org The American Academy of Pediatrics, 141 Northwest Point Blvd., Elk Grove Village, IL 60007
  • 2. Pediatric Lead Exposure From Imported Indian Spices and Cultural Powders WHAT’S KNOWN ON THIS SUBJECT: Lead is a neurotoxin, and AUTHORS: Cristiane Gurgel Lin, MD, PhD,a,b,c Laurel Anne elevated BLLs in children are a public health concern. Immigrant Schaider, PhD,d Daniel Joseph Brabander, PhD,e and Alan children are at risk because of additional exposure to imported David Woolf, MD, MPHb,f a culture-specific leaded products. Lead contamination in many Pediatric Residency Program, Department of Medicine, and fPediatric Environmental Health Center, Division of General imported products has not been characterized. Pediatrics, Children’s Hospital Boston, Boston, Massachusetts; bDepartment of Pediatrics, Harvard Medical School, Boston, WHAT THIS STUDY ADDS: We report here lead-poisoning cases Massachusetts; cDepartment of Neonatology, Pediatrix Medical from Indian cultural powders or spices. Imported products Group, Seton Medical Center, Austin, Texas; dDepartment of surveyed contained lead, and chronic exposure could increase Environmental Health, Harvard School of Public Health, Boston, the prevalence of elevated BLLs. These results increase leaded- Massachusetts; and eDepartment of Geosciences, Wellesley College, Wellesley, Massachusetts product awareness and aid lead-poisoning prevention. KEY WORDS pediatric lead poisoning, childhood plumbism, spices, herbal products, cosmetics, religious powders, lead contamination, Indian, sindoor, culture-specific exposure abstract ABBREVIATIONS CDC—Centers for Disease Control and Prevention BLL— blood lead level BACKGROUND: Significant lead poisoning has been associated with FDA—Food and Drug Administration imported nonpaint products. IEUBK—integrated exposure uptake biokinetic model for lead in OBJECTIVES: To describe cases of pediatric lead intoxication from im- children PEHC—Pediatric Environmental Health Center ported Indian spices and cultural powders, determine lead concentra- XRF—x-ray fluorescence tions in these products, and predict effects of ingestion on pediatric NIST—National Institute of Standards and Technology blood lead levels (BLLs). LOD—limit of detection SBET—simple bioaccessibility extraction test PATIENTS AND METHODS: Cases and case-study information were ob- XRD—x-ray diffraction tained from patients followed by the Pediatric Environmental Health ZPP—zinc-chelated protoporphyrin CI— confidence interval Center (Children’s Hospital Boston). Imported spices (n 86) and cultural powders (n 71) were analyzed for lead by using x-ray fluo- www.pediatrics.org/cgi/doi/10.1542/peds.2009-1396 rescence spectroscopy. The simple bioaccessibility extraction test was doi:10.1542/peds.2009-1396 used to estimate oral bioavailability. The integrated exposure uptake bio- Accepted for publication Nov 16, 2009 kinetic model for lead in children was used to predict population-wide Address correspondence to Cristiane Gurgel Lin, MD, PhD, geometric mean BLLs and the probability of elevated BLLs ( 10 g/dL). Neonatology Department, Seton Medical Center, 1201 W 38th St, Austin, TX 78705. E-mail: cristiane.lin@gmail.com RESULTS: Four cases of pediatric lead poisoning from Indian spices or PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275). cultural powders are described. Twenty-two of 86 spices and foodstuff Copyright © 2010 by the American Academy of Pediatrics products contained 1 g/g lead (for these 22 samples, mean: 2.6 g/g FINANCIAL DISCLOSURE: The authors have indicated they have [95% confidence interval: 1.9 –3.3]; maximum: 7.6 g/g). Forty-six of 71 no financial relationships relevant to this article to disclose. cultural products contained 1 g/g lead (for 43 of these samples, mean: 8.0 g/g [95% confidence interval: 5.2–10.8]; maximum: 41.4 g/g). Three sindoor products contained 47% lead. With a fixed ingestion of 5 g/day and 50% bioavailability, predicted geometric mean BLLs for children aged 0 to 4 years increased from 3.2 to 4.1 g/dL, and predicted prevalence of children with a BLL of 10 g/dL increased more than threefold (0.8%–2.8%). CONCLUSIONS: Chronic exposure to spices and cultural powders may cause elevated BLLs. A majority of cultural products contained 1 g/g lead, and some sindoor contained extremely high bioaccessible lead levels. Clinicians should routinely screen for exposure to these products. Pediatrics 2010;125:e828–e835 e828 LIN et al
  • 3. ARTICLES Lead is a neurotoxin that can cause assess lead contamination among var- (2) religious powders (used in reli- permanent neurocognitive deficits in ious commercially available imported gious or cultural practices, not in- children.1–3 The current Centers for Indian spices and ceremonial prod- tended for consumption, not labeled Disease Control and Prevention (CDC) ucts sold in stores in the Boston, Mas- for use as medication). When more blood lead level (BLL) of concern is 10 sachusetts, area, and (3) predict the than 1 store carried the same brand of g/dL, although a BLL of 5 g/dL prevalence of elevated BLLs in children a given product, it was only purchased also may result in cognitive deficits.4–8 caused by chronic exposure to these once. The name, manufacturer, manu- A national objective of Healthy People products by using the integrated expo- facturer’s location, packaging loca- 2010 is to eliminate elevated BLLs in sure uptake biokinetic model for lead tion, lot number, expiration date, store children. As part of this effort, the CDC in children (IEUBK).23 name, and purchase date were re- has worked to identify at-risk popula- corded when available. For compari- tions and nonpaint sources of lead ex- PATIENTS AND METHODS son, 10 types of spices produced by US posure.3,9 Among those at risk are im- Case-Study Information manufacturers were purchased at a migrant children, who are more likely large New England supermarket, al- Case-study information was acquired though in most cases, the country of than US-born children to have an ele- through the review of medical charts origin was not listed. vated BLL through exposure to non- of patients who were referred to the paint lead sources.10,11 Culture-specific To assess variability between lots of Pediatric Environmental Health Center nonpaint lead sources have been iden- the same product, all products that (PEHC) at Children’s Hospital Boston tified, including imported utensils,12 contained 10 g/g lead were repur- from 2006 to 2008 for an elevated BLL. foods such as Mexican tamarind chased for additional analysis. In addi- The cases represent 2% of new pa- candy,13 cosmetics such as kohl14 and tion, 10% of the spices and powders tient referrals to the PEHC. All patients henna,15 and ayurvedic traditional were randomly selected for repur- were asymptomatic. Home environ- medicines16,17 and Mexican digestive chase and reanalysis. ments were assessed for lead by the remedies.18 Massachusetts Department of Public Culture-specific lead sources have Heavy-Metal Analysis Health via dust wipe and direct sam- placed South Asian and Indian commu- pling of surfaces and by the PEHC via Samples were labeled with a numeri- nities at risk. Woolf and Woolf19 re- environmental inventory and soil- cal identifier only. Four grams of each ported 2 cases of pediatric lead poi- testing. In all cases, no other signifi- sample were transferred into x-ray flu- soning from imported Indian spices. In cant sources of lead were found. orescence (XRF) analytical cups (Pre- addition, a Thai infant suffered lead mier Lab Supply, Port St Lucie, FL) with poisoning from a powder applied to his Collection Methods: Market-Basket 4- m windows (Spex Certiprep, tongue,20 and an Indian child devel- Survey Metuchen, NJ) after thorough homog- oped an elevated BLL from ingestion of In this article, we use the terms “cul- enization. Repurchased products re- sindoor (a powder applied to a wom- tural powder,” “religious powder,” and ceived new numerical identifiers, and an’s scalp as a marriage sign).21 Re- “ceremonial powder” interchangeably. 2 aliquots of each repurchased prod- cently, the US Food and Drug Adminis- Collection and analysis of spices and uct were analyzed. tration (FDA) recalled a brand of powders were based on the protocol The concentration of lead in each sam- ceremonial Indian powders because of outlined by Saper et al.16 Boston-area ple was determined by using a Spectro lead contamination and confirmed stores that sell spices and religious XEPOS polarized energy-dispersive XRF cases of lead poisoning.22 powders were identified through an instrument (Spectro Analytical, Kleve, To date, few studies have systemati- online national directory of Indian gro- Germany). Measurement accuracy cally investigated the lead content of cery stores24 and a New England area was determined by using a standard imported Indian spices and ceremo- Indian community business directo- reference material (National Institute nial powders and considered related ry.25 In early 2008, 15 randomly se- of Standards and Technology [NIST] risks posed to children living in the lected stores were visited within 20 2709, San Joaquin [California] soil).26 United States. The goals of our investi- miles of Children’s Hospital Boston. The measured mean lead concentra- gation were to (1) describe recent Spices and ceremonial powders were tion for NIST 2709 (18.5 0.9 g/g; n cases of pediatric lead poisoning purchased if they were manufactured 48) was consistent with the certified caused by contaminated Indian spices in India and were (1) spices/foodstuffs value (18.9 0.5 g/g). The limit of and religious powders, (2) survey and (edible, used in food preparation) or detection (LOD) is 1.0 g/g. PEDIATRICS Volume 125, Number 4, April 2010 e829
  • 4. Because many spice samples were be- IEUBK Modeling hemoglobin level of 11.2 g/dL, and low the XRF LOD, total lead concentra- The IEUBK model, Windows version 1.0, hematocrit level of 31.7%. He received tion was also determined in a subset of build 264 (US Environmental Protec- 5 days of parenteral chelation with spices by using microwave digestion in tion Agency, Washington, DC), is a nu- intravenous Na2CaEDTA. His zinc- concentrated nitric acid followed by in- merical blood lead predictive mod- chelated protoporphyrin (ZPP) level ductively coupled plasma mass spec- el.23,31 The IEUBK model estimates was elevated at 152 mol/mol of heme trometry (Elan 6100 [Perkin Elmer, population-level BLLs on the basis of (normal ZPP level, based on a hemato- Shelton, CT]) analysis. The LOD is various lead-exposure sources, uptake crit level of 35%: 25– 65 mol/mol), 0.03 g/g. Average recovery of lead via inhalation or ingestion, and bioki- which suggested chronic lead expo- from NIST 1515 (apple leaves) was 88% netics. Probability distributions are sure. The parents described rubbing a (n 2). used to estimate variability in BLLs religious powder on the patient’s fore- among exposed children.23 The IEUBK head since he was several weeks old. Bioaccessibility Analysis They did not add powders to foods. model has been widely used since 1994 For a random subset of samples, lead Lead analyses revealed 89 000 g/g and independently validated and veri- bioaccessibility (ie, fraction of metal lead in the religious powder and 300 fied.32 Because it has been used to es- mobilized in a biologically relevant g/g lead in an eye cosmetic. The par- timate mean BLLs and predict the fluid) was estimated by using the sim- ents stopped using the powder, and probability of elevated BLLs in a popu- the child received oral chelation with ple bioaccessibility extraction test lation of children exposed to lead- dimercaptosuccinic acid for 6 months, (SBET). The SBET is an in vitro gastric contaminated tamarind candy,33 the which reduced the BLL to 21 g/dL. fluid extraction that simulates metal model was considered appropriate for By 21 months of age, the child’s BLL dissolution in the stomach and has the goals, age ranges, and exposure du- was stable (15 g/dL), and he required been shown to predict in vivo lead ab- ration for our population of concern. no additional oral chelation therapy. sorption in juvenile swine, a model for We used the IEUBK model to estimate gastrointestinal absorption in chil- the geometric mean BLL for a popula- Case 2 dren.27,28 The SBET was performed by tion and to predict the probability of A 9-month-old Indian boy was referred following a previously published proto- elevated BLLs caused by intentional for an elevated BLL (21 g/dL). The par- col.29 Bioaccessibility was calculated or accidental ingestion of lead- ents described applying an orange as extracted lead concentration/total contaminated spices or powders. Lead powder (orange shringar) to his fore- lead concentration. exposure from other environmental head as a religious tradition. They did To determine the crystalline phases sources was held constant, and stan- not add powders to food. Lead analy- linked with high-lead sindoor products dard model inputs, comparable to Bos- ses revealed 220 000 g/g in the pow- ( 47% lead), x-ray diffraction (XRD) ton background levels,26,34,35 were used der and 49 g/g in both holy ash and analyses were conducted by using a to incorporate background lead expo- kumkum. Analyses of family spices and rotating copper anode RU 300 genera- sure. Diet inputs were calculated from utensils did not detect lead. The par- tor (Rigaku, Tokyo, Japan). Resulting FDA food-monitoring data.36 For model ents stopped using the powders, and 4 XRD patterns were fit by using Jade runs, an alternate exposure function weeks later the patient’s BLL was 17 software (Materials Data, Livermore, was used to model additional ingestion g/dL, with a ZPP level of 85 mol/mol CA) with search/match of the FIZ- of spices or powders. Bioaccessibility, and hemoglobin level of 10.7 g/dL. Two Inorganic Crystal Structure Database based on SBET data, was used as an months later, his BLL decreased to 13 (http://icsd.ill.eu/icsd/index.html) and upper-bound estimate of bioavailability g/dL. No chelation was administered. Rietveld whole-pattern fitting. XRD (ie, fraction of lead that is absorbed and analyses provide both phase identifi- reaches the systemic circulation).28,37 Case 3 cation and the general bonding envi- A 3-year, 9-month-old Indian girl was ronment of lead. Combining XRD char- RESULTS referred for an elevated BLL (18 g/ acterization with SBET analysis is an Case Summaries dL), a ZPP level of 88 mol/mol, and a effective and underutilized approach hemoglobin level of 10.9 g/dL. No con- to evaluating the chemical form and Case 1 taminated herbs, spices, or ethnic relative solubility of lead in various ex- A 10-month-old Indian boy was re- remedies were discovered. However, a posure media (soils, spices, religious ferred for an elevated BLL (43 g/dL), a religious powder ingested regularly by powders).30 mean corpuscular volume of 69.7 fL, the patient contained 4800 g/g lead. e830 LIN et al
  • 5. ARTICLES TABLE 1 Examples of Cosmetics, Hair Products, and Ceremonial Powders Purchased tistical analysis (Table 3). These sin- Product Name Brand Name Uses door lead concentrations are compa- Cosmetics and hair products rable to those in published reports.21,38 Aritha powder Hesh Shampoo Cosmetics and ceremonial powders Henna Al-aroosa, Ancient Secret, Ayur, Dulhan Hand decoration Kajal Shingar Ltd, Western Indian Chemical Co Eyeliner had similar lead concentration and Hairwash Meera Shampoo ranges (Table 3). Sandalwood Nirav Cosmetic, medicinal Ceremonial powders Abil Bhavani, Nirav Pooja ceremony Indian Spices and Foodstuff Gulal MDHD, Swad, Durbar Pooja ceremony Eighty-six food products manufac- Kumkum Shringar, Topaz, Butala Emporium Bindi Sindoor MDHD, Swad, Nirav, Butala Emporium Marriage symbol tured by 53 companies were pur- chased (Table 2). Sixty-three prod- ucts listed packaging location, and 38 The family discontinued use of this seed (0.6 g/g), asafoetida (0.8 g/g), products listed lot numbers. Thirty- powder, and over the next 8 months, and turmeric (1.4 g/g). The family eight products were categorized as the patient’s BLL decreased to 8 g/dL. discontinued use of all imported common spices, used daily in food spices, and the patient’s BLL declined preparation, whereas 48 were catego- Case 4 to 14 g/dL within 6 months. rized as foodstuff, including spice A 12-month-old Indian boy was re- mixes, food coloring, or other food ad- ferred for an elevated BLL (28 g/dL), a Religious Powders ditives, which may be used less fre- ZPP level of 103 mol/mol, and a hemo- Seventy-one religious products manu- quently. Of the 86 products tested by globin level of 9 g/dL. Analyses of factured by 28 companies were pur- XRF, 22 (26%) contained 1 g/g lead, spices, herbal remedies, and religious chased (Table 1). Forty-three products with a mean lead concentration in powders revealed that several Indian listed packaging location, and 5 prod- these 22 samples of 2.6 g/g (95% CI: spices, used daily, contained lead: an ucts provided lot numbers. Sixteen 1.9 –3.3) and a maximum of 7.6 g/g herb mix (11 g/g), brown mustard products were categorized as cosmet- (sea salt). Food products had a lower ics and hair products for daily use, and percentage of samples with detected 55 were categorized as ceremonial re- lead and lower mean lead concentra- TABLE 2 Examples of Spices and Foodstuff Purchased ligious powders for daily to monthly tion compared with religious prod- Product Name Brand Name use. ucts. Spices and foodstuff contained Spices Of the 71 cultural products tested, 46 similar ranges of lead concentration Black pepper Laxmi, Swad, Deep (65%) contained 1 g/g lead. The (Table 3). Cardamom DEEP Chili powder Saras, Noer, Swan mean lead concentration in 43 sam- On the basis of a direct comparison of Coriander MDHD, Periyar, Swad, Swan ples with detectable lead (excluding 3 10 types of spices (US brands and im- Fennel powder Deep high-lead sindoor products) was 8.0 ported) analyzed by inductively cou- Fenugreek Swad g/g (95% confidence interval [CI]: pled plasma mass spectrometry, im- Garam masala MDHD, Swan Garlic power Shalimar 5.2–10.8 g/g), with a maximum of ported spices had a mean lead Ginger powder Himgiri, Swad 41.4 g/g (kajal). Three sindoor prod- concentration of 0.5 g/g (95% CI: Paprika Swad 0.18 – 0.72), which was twice the mean ucts contained 47% lead by weight Sindav salt Deep, Swad Turmeric Laxmi, Nirav, Swad, Swan and were treated separately in the sta- lead concentration of US-brand spices Foodstuff Food coloring Bush, Bhavani, Narmada, Vesco TABLE 3 Mean Concentration, CI, and Range of Lead in Spices, Foodstuff, Cosmetics, Ceremonial Dabelli masala Bombay Magic Powders, and High-Lead Sindoor With a Detectable Lead Level by XRF Fish curry MDH Product No. of Samples With Lead Level, Mean Range, g/ga Vada mix MTD Samples Detectable Lead, % (95% CI), g/ga Chappli kabab Roopak Spices 38 24 2.6 (1.2–4.0) 1–7.6 masala Foodstuff 48 27 2.6 (1.8–3.4) 1–6.3 Vermacelli mix MTR Cosmetics 16 81 7.6 (1.3–13.9) 1–41.4 Tulsi powder Bhavani Ceremonial powders 52 58 8.2 (6.0–10.4) 1–39.9 Karela powder Swad High-lead sindoor 3 100 559 000 (463 000–655 000) 469 000–638 000 Asafoetida Laljee Godhoo, Ruchi, Swad a Serial dilutions of NIST 2709 suggest that the LOD (based on the criteria that samples run in triplicate maintain 10% Amchur powder Deep relative SD) is 1.0 g/g (data not shown). LOD estimates based on serial dilution of NIST 2709 were supported by 15 replicate Hajmola candy Dabur India Ltd analyses of NIST 1515 (apple leaves) in which a 20% SD was observed for an expected lead concentration of 0.47 g/g. PEDIATRICS Volume 125, Number 4, April 2010 e831
  • 6. (0.19 g/g [95% CI: 0.1– 0.28]) (Table form of lead in these samples. Minium for children aged 0 to 4 years in- 4). However, this difference was not is commonly used as a pigment in creased from 3.2 to 4.1 g/dL, and the significant on the basis of a pairwise t henna and lead paint.15,43 predicted prevalence of children with test (P .1). The lead concentration in an elevated BLL increased threefold, these 10 imported spices was up to IEUBK Modeling from 0.8% to 2.8%. The difference is fivefold higher than the recommended The IEUBK model was used to predict more dramatic with small increases in maximum level in hard candy (0.1 g/ the effects of chronic ingestion of ingested amount and bioavailability g).39 In addition, imported spices had a spices or religious powders on popula- (Figs 1 and 2); at 5 g/day and 80% similar range of lead concentrations tion BLLs. For a fixed ingestion rate bioavailability, 4.9% of children were as spices manufactured in Pakistan ( g/day), the geometric mean BLL and predicted to have an elevated BLL, and (0.02–9.2 g/g).40 Although the FDA has percentage of children with an ele- at 10 g/day and 50% bioavailability, no recommended maximum lead con- vated BLL (defined as a BLL of 10 g/ 6.5% of children were predicted to centration for spices, the European dL) were calculated. When the model have an elevated BLL. These results Union’s recommended limit for dried was run with default inputs only, the suggest that infants and children can herbs is 2 to 3 g/g.41 background geometric mean BLL for develop lead poisoning by chronic in- children aged 1 to 5 years was 3.1 g/ gestion of contaminated spices and Bioaccessibility dL. This value is higher than the na- ceremonial powders. We determined bioaccessibility for a tional geometric mean BLL of 1.9 g/dL subset of samples by SBET as a reason- but comparable to that of black chil- DISCUSSION able approximation for bioavailabil- dren (2.8 g/dL) and children in low- Our analyses demonstrate the risk of ity.28 Spices had a mean lead bioacces- income households (2.5 g/dL).44 The lead poisoning associated with con- sibility of 49% (95% CI: 32– 66) (Table percentage of children with an ele- taminated ceremonial powders and 5), which is consistent with previously vated BLL (0.6%) was lower than the rituals that involve the external appli- published data37,42 and with the default national average (1.6%).44 Overall, these cation of these powders to young in- IEUBK value of 50% for lead absorption data suggest that the model can reason- fants. Of particular concern are (1) the from food.37 Religious and cosmetic ably approximate background BLL for extremely high lead concentrations products and sindoor (with 47% children who live in the United States. found in some readily available sin- lead) had similar mean lead bioacces- To model increased exposure resulting door powders (47%– 64% lead), (2) the sibility (50%–56%) as spices (Table 5). from spice or accidental powder inges- moderate lead concentrations found XRD results indicated that Pb3O4 tion, we used a fixed lead-ingestion rate in other cultural powders (up to 40 g/ (minium, “red lead”) is the chemical (5 g/day). Spice-ingestion rates for g), (3) the young age at which parents various lead concentrations are listed commence such practices, and (4) the TABLE 4 Mean Concentration, CI, and Range in Table 6 and are comparable to those chronic nature of the exposure (up to of Lead in US-Brand Spices and in published reports.45,46 When the several times per week). Although the Indian Brand Spices (N 10) model was run with a fixed ingestion powders are not meant for consump- Producta Lead Level, Mean Range, (95% CI), g/g g/g rate of 5 g/day and 50% bioavailabil- tion, we speculate that infants may be US brands 0.19 (0.1–0.28) 0.03–0.41 ity, the predicted geometric mean BLL inadvertently exposed by hand-to- Indian brands 0.45 (0.17–0.73) 0.12–1.54 mouth transference of topically ap- a Spices tested included garlic powder, black pepper, fen- plied powders or by the hands of par- nel powder, ginger powder, coriander, garam masala, tur- ents who handle the powder and then TABLE 6 Ingestion Rate as a Function of Lead meric, chili powder, paprika, and cardamom. Concentration for Lead Ingestion of prepare foods for the infant’s con- 5 g/g sumption. Infants may also be exposed Lead Daily Ingestion Weekly TABLE 5 Mean Bioaccessibility, CI, and Range to these products in utero, through of Bioaccessibility of Religious Concentration, Ratea Ingestion Rate Powders, Spices, and High Lead g/g g Teaspoons g Teaspoons breastfeeding, inhalation of aerosol- Sindoor ized particles, or dermal absorption.12 0.5 10 2 70 14 Product No. of Mean Range, 1 5 1 35 7 As predicted by IEUBK modeling, Samples Bioaccessibility, % 5 1 0.2 7 1.4 10 0.5 0.1 3.5 0.7 chronic exposure can have a dramatic % (95% CI) 20 0.25 0.05 1.75 0.35 effect on BLL. For instance, ingesting Powders 6 56 (20–92) 20–80 Spices 10 49 (32–66) 22–100 a Mean ingestion rate of spices in g/day for children aged 20 g of high-lead sindoor increases 1 to 3 years, living in India, was reported to be 5 g/day, with High-lead 3 50 (38–62) 40–62 a range of 3 to 10 g/day, as reported by the National Nutri- lead exposure by 10 g/day and the sindoor tion Monitoring Bureau.45,46 probability of elevated BLL by eightfold. e832 LIN et al
  • 7. ARTICLES ated. Such items include cosmetics, such as kohl,14 and we now extend the product list to include Indian powders intended for use in reli- gious practices. We also found that under certain cir- cumstances, exposure to imported In- dian spices may increase the preva- lence of elevated BLL. IEUBK modeling predicted that chronic ingestion of spices that contained our highest mea- sured lead concentration (7.6 g/g) may result in elevated BLLs. Therefore, a risk for lead poisoning exists if there is sufficient lead contamination or a high daily dose. This risk is not theoret- ical, as indicated by our case report of lead poisoning from chronic ingestion of imported spices with similar lead FIGURE 1 concentrations (1–11 g/g). The IEUBK model was used to predict mean geometric BLLs in children aged 0 to 4 years with varying exposures. In this simulation, daily lead ingestion and bioavailability were varied, and resulting BLLs There are several limitations of our are shown. study. First, although we analyzed more than 150 products, our samples did not represent all types of Indian- manufactured products. Second, there may be lot-to-lot variability in lead concentration depending on manu- facturing and packaging practices and on natural spice-plant accumu- lation of lead. Third, regional varia- tion in Indian product availability and distribution may limit the applicabil- ity of the study to other locations. Fourth, family usage patterns will af- fect the overall cumulative exposure and risk of injury. We did not acquire end-user information regarding these products. Nevertheless, to our knowledge, our study represents the FIGURE 2 first attempt to investigate a variety The IEUBK model was used to predict the prevalence of BLLs of 10 g/dL in a population of children of cultural products and to carefully aged 0 to 4 years with varying exposures. In this simulation, daily lead ingestion and bioavailability were varied. consider their potential effects on pediatric BLL. Ingestion of 250 mg of sandalwood, an studies have shown risks to children CONCLUSIONS amount comparable to pediatric soil from remedies, foods, and spices Our investigation of Boston-area ingestion through hand-to-mouth ac- meant for consumption,16–19,48 lead stores that sell Indian spices and reli- tivities,47 increases exposure by 5 g/ poisoning from contaminated prod- gious powders revealed a ready avail- day and the probability of elevated ucts intended only for external appli- ability of lead-contaminated items. BLL by threefold. Although previous cation has not been fully appreci- Similar products can also be pur- PEDIATRICS Volume 125, Number 4, April 2010 e833
  • 8. chased on the Internet. Furthermore, itored, and low-lead sindoor ( 5 pretation of the data; or preparation, we were able to purchase highly con- g/g) could be suggested as a safer review, or approval of the manu- taminated items that were previously alternative. Closer inspection and script for submission. banned or recalled by the FDA. The high testing of other religious products is Ms Suzanne Giroux (PEHC, Children’s prevalence, availability, chronic and warranted. Hospital Boston) assisted in ascertain- widespread use,49 and potential toxic- ing the clinic families identified for in- ACKNOWLEDGMENTS ity of these products pose a public clusion in the case series. James Be- Dr Lin was supported by the Lovejoy health risk. Clinicians should be aware sancon, PhD (associate professor of Residency Research Fund (Children’s of these and other imported hazards Hospital Boston). Dr Woolf was sup- geosciences at Wellesley College) con- and inquire about their use during rou- ported in part by a grant from the ducted the XRD analyses on the sin- tine health supervision visits. Further- Agency for Toxic Substances and Dis- door samples. Ms Emily Estes, Ms more, per CDC and American Academy ease Registry Superfund Reconcilia- Nooreen Meghani, and Ms Megan of Pediatrics recommendations, clini- tion and Reclamation Act, adminis- Carter-Thomas (Wellesley College) as- cians who work with South Asian com- tered through the Association of sisted with XRF sample analysis and munities should perform targeted BLL Occupational and Environmental Clin- assessment of standards performance. screening on new immigrants and rou- ics Association (Washington, DC). Chil- Ami Zota, ScD (Program on Repro- tinely administer lead-exposure risk- dren’s Hospital Boston, Harvard Medi- ductive Health and the Environment, assessment questionnaires (provided cal School, Harvard School of Public University of California, San Fran- by state departments of health50,51), Health, Wellesley College, Stanford Uni- cisco, CA) and Ananya Roy, ScD (De- modified to include these hazards.52,53 versity School of Medicine (Dr Lin’s partment of Health Sciences, School Because of the high lead concentra- former affiliation), and Pediatrix of Public Health, University of Michi- tions found in some sindoor sam- Medical Group had no role in the de- gan, Ann Arbor, MI) reviewed earlier ples, import, sale, and labeling of sign or conduct of the study; collec- drafts of this manuscript. None re- these items should be carefully mon- tion, management, analysis, or inter- ceived compensation. REFERENCES 1. Tong S, Baghurst PA, Sawyer MG, Burns J, children and adolescents. 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