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Published in final edited form as:

Pediatr Infect Dis J. 2012 November ; 31(11): 11441147. doi:10.1097/INF.0b013e318266b6c4.

Pediatric Tuberculosis: The Litmus Test for Tuberculosis

Control
Lucila Marquez, MD, MPH1, Marsha L. Feske, PhD, MPH2, Larry D. Teeter, PhD2, James M.
Musser, MD, PhD2, and Edward A. Graviss, PhD, MPH2
1Department of Pediatrics, Section of Infectious Diseases, Baylor College of Medicine, Houston,
Texas, USA
2Department

of Pathology and Genomic Medicine/ Molecular Tuberculosis Laboratory, The

Methodist Hospital Research Institute, Houston, Texas, USA

Abstract
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BackgroundThe epidemiology of pediatric tuberculosis (TB) from 19952000 in Harris

County, TX has been previously reported. This study was conducted to evaluate the continued
trends of Mycobacterium tuberculosis (MTB) clustering and the role of genotyping in pediatric
TB.
MethodsData came from the Houston Tuberculosis Initiative, a prospective population-based
active surveillance and molecular epidemiology project. The study population consisted of TB
patients 18 years of age diagnosed in Harris County, TX from 2000 to 2004. Available MTB
isolates were characterized by IS6110 restriction fragment length polymorphism and
spoligotyping.
Results103 pediatric TB cases were enrolled in the Houston Tuberculosis Initiative study from
20002004. Sixty-one (59%) patients had potential source cases. MTB isolates were available and
genotyped for 36 pediatric cases; 27 (75%) were clustered into 22 different genotypes. Of the 20
genotyped patients with a potential source case, 16 (80%) were clustered. Genotypes matched the
potential source case in 12 cases. Eleven of the 16 (69%) genotyped patients without a potential
source case were clustered.

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ConclusionsCompared with pediatric cases in 19952000, there was a significant increase in

the number of patients with unknown potential source cases that were clustered within the
Houston Tuberculosis Initiative database. Since genotypic clustering is associated with recent
transmission, there appears to be a failure in the identification of potential source cases through
contact tracing. Reduced funding of public health departments forces more limited TB control
activities and therefore could pose a threat to TB control.
Keywords
tuberculosis; pediatric; genotype; cluster

Corresponding Author: Lucila Marquez MD; 1102 Bates Ave. Suite 1120, Houston, TX, 77030; tel: 832-824-1780; fax:
832-825-4347; [email protected].
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Conflicts of interest For the remaining authors, none were declared.

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Introduction
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Harris County, TX contributes significantly to not only the overall national burden of
tuberculosis (TB), but also to pediatric TB cases. In terms of annual TB case counts by city,
Houston ranks second behind New York. In the Houston Metropolitan Statistical Area, 402
cases of adult and pediatric TB were confirmed in 2010 accounting for a case rate of 6.7 per
100,000. 1 This was nearly twice the national average of 3.6 cases per 100,000 in the same
year. As far as pediatric cases, between 1993 and 2006, 12 % of all US pediatric cases came
from Texas 2 and in 2010 the Houston Metropolitan Statistical Area had the second highest
number of TB cases among children younger than 5 years of age.1
The Centers for Disease Control and Prevention (CDC) recommends that control of TB in
children and adolescents receive high priority. Because a case of tuberculosis in an infant
and young child is inherently due to recent transmission, pediatric cases often direct TB
control programs to an adult in the community that is actively transmitting disease. In as
much, children are an important component of TB eradication programs and have proven to
be markers for TB transmission within communities.3

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Wootton et al. 4 reported the epidemiology of pediatric TB in Harris County, TX from

10/1/19959/30/2000. This study questioned the accuracy of traditional contact
investigations and highlighted that molecular characterization of TB isolates may help
identify source cases. We conducted this study to evaluate the continued trends in clustering
of pediatric TB in Harris County, TX. Our study goal was to determine the role of
genotyping in the identification of source cases for pediatric TB.

Materials and Methods

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Available data was reviewed from the Houston Tuberculosis Initiative (HTI), a prospective
population-based active surveillance and molecular epidemiology project. The HTI enrolled
Harris County TB patients reported to the City of Houston Department of Health and
Human Services and Harris County Public Health and Environmental Services from October
1, 1995 through September 30, 2004 (hereafter referred to as 1995 to 2004) and captured
85% of patients reported to these agencies.5 The current study population consisted of TB
patients who were 18 years of age and younger, counted in Harris County, TX from October
1, 2000 to September 30, 2004 (hereafter referred to as 2000 to 2004). Cases or parental
proxies were interviewed using a standardized questionnaire. Available Mycobacterium
tuberculosis (MTB) isolates were characterized by insertion sequence (IS) 6110 restriction
fragment length polymorphism (RFLP) using an internationally standardized method and
results were analyzed with the BioImage Whole Band Analyzer software version 3.2
(BioImage, Ann Arbor, MI). Genotype information was supplemented with spoligotyping to
discriminate among isolates with 5 or fewer IS6110 copies.6 Spoligotype families were
identified by matching the octal code to the SPOLDB4 database.7
Geographic Information Systems tools were used to assess for any geographic clustering,
within previously identified genotypic MTB clusters and spatial autocorrelation with risk
factors associated with TB transmission. These risk factors included bus-ridership, a
covariate shown previously to be associated with HTI Homeless TB cases and census tracts
with endemic TB in Harris County.8
Definitions
Cases were considered clustered if their TB isolate matched another isolate in the HTI
database with an identical number of bands and molecular weight pattern by RFLP, and
among isolates with 5 or fewer IS6110 copies, matching spoligotypes.

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A potential source case (PSC) was defined by public health and/or HTI interviews as a close
contact to a case patient who carried a diagnosis of tuberculosis disease. Cases were
considered to have geographic proximity if they shared the same zip code.
Case definitions included: laboratory-confirmed, clinical case, or provider diagnosis.
Laboratory confirmation signified that the organism was isolated by culture, PCR, or acidfast bacilli were observed in pathologic specimens. Clinical criteria included a positive
tuberculin skin test, clinical findings consistent with TB, and treatment with at least 3 antiTB drugs. Provider diagnosis was at the discretion of the clinician but in general followed
criteria set forth by the American Academy of Pediatrics.9
Data were analyzed using Stata 10 (Stata Corp. 2007, College Station, TX). Categorical
variables were compared using the 2 test, logistic regression or Fischers exact test when
appropriate. All p-values were 2-sided with = 0.05 as the significance level.

Results

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Between 2000 and 2004, 121 pediatric TB patients were reported to the Harris County
public health departments. Eighteen patients were excluded because they were prevalent
cases (n = 4), unable to be located (n = 11), and refused interview (n = 3). Thus, 103
pediatric TB cases were enrolled in the HTI study. The characteristics of the pediatric cases
are listed in Table, Supplemental Digital Content 1, http://links.lww.com/INF/B280. Fortyseven percent of cases were younger than 5 years-old. Females represented 52% of cases.
Sixty-three percent of cases were Hispanic and the majority (81%) of cases were US-born.
One-half of patients had extra-pulmonary sites of disease. Two case isolates were drug
resistant, isoniazid-monoresistant and isoniazid/streptomycin, respectively. Contact
investigations or HTI interviews were able to identify that sixty-one patients had a potential
source case. Table 1 summarizes the characteristics of pediatric TB cases with and without
an identified source case. Having a PSC was associated with younger age and US birth.

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MTB isolates were available from only 41 (40%) cases and 36 (35%) were genotyped.
Twenty-seven (75 %) genotyped cases were clustered into 22 different molecularly
characterized IS6110 groups within the 19952004 HTI database (Table 2). At least eight of
27 (30%) clustered isolates belonged to the Beijing family; other lineages are shown in
Table 2. Three of the 22 genotypes had more than 1 pediatric case, with the largest pediatric
representation in one cluster being 3 patients. The median size of the 22 HTI clusters was
7.5 with matched genotypes, with a range of 2 to 122 cases per cluster. Of the 22 MTB
clusters, 7 were not identified by HTI between 1995 and 2000. Thus, 7 clusters that involved
pediatric patients were new to HTI between 2000 and 2004. Of the 7 pediatric cases in
new clusters, 5 had a potential source case.
Of the pediatric patients with a PSC between 2000 and 2004, 16 patients were clustered
(Figure, Supplemental Digital Content 2, http://links.lww.com/INF/B281). Matching
between the genotype of the pediatric patient and the PSC occurred in all 12 cases for which
genotypes were available for both the patient and source.
Of the 27 clustered pediatric cases, the age distribution was as follows: 11 were 04 yearolds, two were 59 year-olds, four were 1014 year-olds, and 10 were 1518 year-olds. The
age distribution of clustered patients was bi-modal, with nearly 80% of cases being in the
age groups 04 years-old or 1518 years-old.
Eleven patients without a PSC were clustered. We further evaluated if epidemiologic links
existed within clusters that included a pediatric case that did not have a public health
reported source case (Table 3). The 11 cases fell into 9 clusters, of which 4 had direct
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epidemiologic links which could be discerned. In another 4, possible epidemiologic links

existed, including geographic proximity, shared bus routes, and the risk factor of
homelessness. We could not find any epidemiologic links in 1 cluster (H040).
In cluster H218, there were a total of 7 patients across all HTI years. All cases in this cluster
were either born in Vietnam or had Vietnamese parents. Direct epidemiologic links were
found between 4 cases in this cluster. Three pediatric cases between 2000 and 2004
belonged to this cluster, 2 of whom did not identify a contact. One of these cases was an 18
year-old male born in Vietnam. Both pediatric cases in cluster H218 without a source case
lived in the same zip code. Additionally, they shared a zip code with another US-born
clinically-diagnosed pediatric case presumed to have been infected by his/her Vietnamese
mother who belonged to this cluster.

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Cases in cluster H147 were primarily Hispanic. Of 15 cases, 13 (87%) were Hispanic and 6
(40%) reported being born in Mexico. Cluster H147 contained 2 US-born pediatric cases
without a named/known source. Six other cases in this cluster had a direct epidemiologic
link to at least another case in this cluster; these had morbidity dates within an 18 month
period of each other. One of the pediatric cases belonging to this cluster was a 4 month-old
infant, whose mother reported the child rode a public transport bus one or more times a
week. This infant shared a bus route with at least one other adult member of this cluster. The
individual with whom the child shared the bus route was deemed to have been infectious for
a period of 127 days. This potential source case had TB risk factors including homelessness
and incarceration.
One pediatric case without a source belonged to cluster H007, which principally comprised
US-born individuals. The child in this cluster was Hispanic, but 58% of the cases were
African-American. At least 17 of the 85 cases in this cluster had a direct epidemiologic link
to at least another case in this cluster. In cluster H014, 6 cases had a direct epidemiologic
link to at least another case in this cluster.
The pediatric case in cluster L024 shared a zip code with an adult in the cluster. The 2 adults
in cluster H231 had the shared risk factor of homelessness. In cluster L028, the pediatric
case shared a bus route with 2 adult cases that were infectious for 100+ days. The 15 yearold patient in cluster L007 was geographically clustered with 2 other cases that were
diagnosed 2 years prior.

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In the n-1 method described by Small et al.9, the index case is subtracted from the cluster
size to obtain the number of cases presumed to be due to recent transmission. Between 1995
and 2004, 577 cases belonged to the 22 clusters that involved pediatric patients. Using the
n-1 method, 555 were due to recent transmission.

Discussion
In the first 5 years of the HTI, 220 of 2242 (10%) cases were 18 years-old. In the
subsequent 4 years, 103 of 1306 (8%) were 18 years-old, a significant decrease in the
proportion of pediatric TB cases (p = 0.048). Hispanics were overrepresented when
considering both the demographics of Houston and the demographics of pediatric cases
throughout the United States. Sixty-three percent of the pediatric cases during our current
study were Hispanic. In comparison, 46% of children in Harris County, TX (http://
txsdc.utsa.edu/tpepp/2004ASREstimates/alldata.pdf) and 39% of national pediatric TB cases
were Hispanic.11
Between 1995 and 2000, 7 of 78 (9%) of isolates were resistant to at least one drug vs. 2 of
41 (4.9%) in the current portion of the study (p= 0.42).
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The CDC defines recent transmission as a transmission event occurring within the previous
2 years.12 Genotyping offers an additional means of distinguishing cases of tuberculosis due
to recent transmission from cases that are due to reactivation. The CDC National
Tuberculosis Genotyping Service now uses spoligotyping and 24 loci mycobacterial
interspersed repetitive units variable number tandem repeat typing to characterize isolates
followed by RFLP in certain circumstances.12 Data from the National Tuberculosis
Genotyping and Surveillance Network indicate that spoligotyping alone is not able to
distinguish isolates that are common in the United States, including the Beijing and T1
families. Thus, it is of benefit to use RFLP to characterize isolates and imperative that a
second PCR-based method such as mycobacterial interspersed repetitive units be used in
molecular characterization.12
Matching of genotypes does not automatically imply that cases are involved in the same
chain of transmission, especially in areas with moderately high prevalence of Beijing family
strains such as Houston.6 There must be epidemiologic links that can explain where and
how they might have transmitted TB among themselves.12 Epidemiologic links could
include living, working or spending time in the same location, social networks, sharing of
risk factors, and the infectious period.12

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In young children who tend to have rapid progression from infection to disease, pediatric
tuberculosis is suggestive of recent transmission. Most TB experts also believe clustering
signifies recent transmission.10 If a significant portion of pediatric cases are clustered, this
lends more credence to the fact that cases of pediatric tuberculosis result from recent
transmission. We found that 27 of 36 (75%) of pediatric cases from 20002004 who had
isolates subjected to molecular characterization were clustered. In comparison, when TB
transmission dynamics were evaluated in adults in Houston for the years 19961998, 666 of
1131 (59%) of cases were clustered and 52% were thought to occur due to recent
transmission.13 The trend suggests a higher proportion of clustering in pediatric patients
(p=0.054). The evolution of new clusters in the HTI database further supports ongoing
transmission of tuberculosis in Harris County, TX.

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Much like in our study, the proportion of clustered cases in the pediatric population in Harris
County between 1995 and 2000 was 72%. This is not an encouraging figure given that
improved control of tuberculosis should lead to declines in clustered cases. However, in the
current study, 11 of 16 (69%) genotyped cases without a source case were clustered with as
many as 85 other cases in Harris County. In contrast, between 1995 and 2000, only 4 of 25
(16%) children without a source case matched via genotyping 1 other adult case in the HTI
database.4 The differences between the 19952000 and 20002004 data are statistically
significant (p < 0.01).
We additionally found that there were no mismatches of genotype between pediatric cases
and potential source cases identified through traditional contact investigations- 12 cases
matched and the genotype of the source case was not available in four cases. This is in
contrast to the data previously reported by Wootton for tuberculosis cases in Harris County,
TX.4 It is also in contrast to other published molecular investigations such as that by the
Massachusetts Department of Public Health that found that 27% of epidemiologic links were
not verified by genotyping. 14
The lineages in clustered pediatric cases are representative of lineages known to circulate in
North America.15 Both Beijing and T1 families are common in the Unites States.12 Over
10% and 20% of North American isolates are of the Beijing family or T1 families,
respectively.15

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Patients without a potential source case who are clustered and have possible epidemiologic
links deserve further investigation to confirm the epidemiologic links. In Maryland, cluster
investigations that occurred after genotyping results were available helped establish 30%
more epidemiologic links than traditional contact investigations.16 Identification of these
cases aided in halting continued transmission by identifying cases early. The CDC has
ranked by priority the scenarios that warrant cluster investigations. After ruling out falsepositive cultures, investigations of clusters that include high-risk patients warrant the highest
priority.12 High-risk populations include those with increased risk of progression from latent
to active disease, such as pediatric patients. In circumstances where resources are scarce,
enhanced cluster investigations should be conducted when there are more than 2 or 3 cases
in the cluster. Using the strict criteria of more than or equal to 4 cases per cluster, between
1995 and 2004, 15 enhanced cluster investigations should have been conducted. In fact, the
CDC explicitly states that if it is deemed that interviews need to be conducted for cluster
investigations and local resources are insufficient, then it is the states responsibility to
provide those resources.12

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Limitations to this study exist. Data for parents country of origin was not routinely
collected, limiting our ability to assess foreign-born household contacts as a risk factor for
US-born cases. Because isolates were available for only on a few pediatric cases (35%), the
extent of clustering is likely conservatively underestimated. There may be endemic strains in
Houston that are not due to recent transmission but have been circulating within the pool
population for a number of years. The n-1 method assumes clustered cases are due to recent
transmission. However, this may not be the case in a population where characterization has
occurred over ten years and endemic TB cases are known to occur. Thus, the n-1 method
could overestimate associations between cases.

Supplementary Material
Refer to Web version on PubMed Central for supplementary material.

Acknowledgments
sources of funding: The Houston Tuberculosis Initiative was funded in part by the National Institute of Allergy
and Infectious Diseases, National Institutes of Health, under contract N01-A0-02738 and AI 41168. Lucila
Marquez received a travel grant from the American Thoracic Society for an abstract presentation related to this
research.

References
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1. CDC. Reported Tuberculosis in the United States, 2010. Atlanta, GA: US Department of Health and
Human Services, CDC; 2011 Oct.
2. CDC. Epidemiology of Pediatric Tuberculosis in the United States, 19932006. Atlanta, GA: US.
Department of Health and Human Services, CDC; 2006.
3. Controlling tuberculosis in the United States: Recommendations from the American Thoracic
Society, CDC, and the Infectious Diseases Society of America. MMWR Recomm Rep. 2005; 54:1
81.
4. Wootton S, Gonzalez B, Pawlak R, et al. Epidemiology of pediatric tuberculosis using traditional
and molecular techniques: Houston, Texas. Pediatrics. 2005; 116(5):11411147. [PubMed:
16264001]
5. Serpa J, Teeter L, Musser J, Graviss E. Tuberculosis disparity between US-born blacks and whites,
Houston, TX, USA. Emerg Infect Dis. 2009; 15(6):899904. [PubMed: 19523288]
6. Soini H, Pan X, Amin A, Graviss E, Siddiqui A, Musser J. Characterization of Mycobacterium
tuberculosis isolates from patients in Houston, TX by spoligotyping. J Clin Microbiol. 2000; 38(2):
669676. [PubMed: 10655365]

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7. SpolDB4. [http://www.pasteur-guadeloupe.fr/tb/spoldb4]
8. Feske M, Teeter L, Musser J, Graviss E. Giving TB wheels: public transportation as a risk factor for
tuberculosis transmission. Tuberculosis (Edinb). 2011; 91S1:S16S23. [PubMed: 22088323]
9. American Academy of Pediatrics. Tuberculosis. In: Pickering, L.; Baker, C.; Kimberlin, D.; Long,
S., editors. Redbook: 2009 Report of the Committee on Infectious Diseases. 28th ed.. Elk Grove
Village, IL: American Academy of Pediatrics; 2009. p. 680-701.
10. Small P, Hopewell P, Singh S, et al. The epidemiology of tuberculosis in San Francisco: A
population-based study using conventional and molecular methods. N Engl J Med. 1994; 330(24):
17031709. [PubMed: 7910661]
11. Nelson L, Schneider E, Wells C, Moore M. Epidemiology of childhood tuberculosis in the United
States, 19932001: the need for continued vigilance. Pediatrics. 2004; 114:333341. [PubMed:
15286213]
12. National TB Controllers Association/ CDC Advisory Group on Tuberculosis Genotyping. Guide to
the Application of Genotyping to Tuberculosis Prevention and Control. Atlanta, GA: US
Department of Health and Human Services, CDC; 2004 Jun.
13. El Sahly H, Adams G, Soini H, Teeter L, Musser J, Graviss E. Epidemiologic differences between
United States- and foreign-born tuberculosis in Houston, Texas. J Infect Dis. 2001; 183:461468.
[PubMed: 11133378]
14. Miller AC, Sharnprapai S, Suruki R, et al. Impact of genotyping of Mycobacterium tuberculosis on
public health practice in Massachusetts. Emerg Infect Dis. 2002; 8:12851289. [PubMed:
12453357]
15. Brudey K, Driscoll J, Rigouts L, et al. Mycobacterium tuberculosis complex genetic diversity:
mining the fourth international spoligotyping database (SpolDB4) for classification, population
genetics and epidemiology. BMC Microbiol. 2006; 6(23):117. [PubMed: 16401340]
16. Cronin WA, Golub JE, Lathan MJ, et al. Molecular epidemiology of tuberculosis in a low-to
moderate-incidence state: are contact investigations enough? Emerg Infect Dis. 2002; 8:1271
1279. [PubMed: 12453355]

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Table 1

Characteristics of pediatric cases according to potential source case (PSC) status

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PSC
(n= 61)

No PSC
(n = 42)

P-value
(Wald)

6.2, 4

9.1, 8.5

0.026

< 6 months

referent

612
months

0.590

Age (mean, median)

Time living in
Harris County

12 years

0.598

> 2 years

44

33

0.841

Foreignborn

15

0.001

US- born

56

27

5, 2.4

5.3, 4.6

0.367

0.856

Country of Origin,
n (%)

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Time living in the

US (mean, median)

Foreign travel
Yes

No

53

37

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10

H040

H014

H147

H200

L028

H231

H236

H258

H267

H222

L007

L024

L008

L009

H191

H288

H075

29

22

12

15

11

10

13

13

12

18

21

10

20

IS6110
copy
number

N/D

N/D

N/D

647737607760771

N/D

777742777760601

LAM2

777776777760601

777776777760771

777776777760771

777777777720771

000000004020771

777777034020771

776377700160771

776377777760751

777777777760771

777777777760771

777777777760771*

X2

X2

X1

X1

Haarlem 3

Haarlem 2

Haarlem 1

T1

T1

T1

777777777760031

000000000003771

Beijing
U

000000000003771*

000000000003771*

000000000003771

000000000003771

000000000003771

Spoligotype

Beijing

Beijing

Beijing

Beijing

Beijing

Spoligotype
Family

Spoligotyping not done on this patient MTB isolate, designation based on consensus for RFLP- genotype

Spoligotype of at least one isolate in this cluster

Number of Harris County TB Cases with the given cluster designation 19952004

N/D = not done

122

H218

94

42

85

H033

H007

99

H003

Cluster
size

H015

No. of
patients

Cluster

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Genotypes of clustered pediatric cases

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Table 2
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18 y

18 y

5y

6m

15 y

10 y

H014

L024

H231

L028

L007

H040

Hispanic

Hispanic

Hispanic

Hispanic

Hispanic

Hispanic

Hispanic

Hispanic

2y

15 y

H007

Hispanic

Asian

4m

18 y

H147

Asian

7y

H218

Race/
Ethnicity

Age

Cluster

Mexico

El Salvador

U.S.

U.S.

Honduras

U.S.

U.S.

U.S.

U.S.

Vietnam

U.S.

Country of
Origin

2 (1)

22 (1)

12 (1)

3 (1)

29 (4)

8 (2)

85 (3)

15(3)

15(3)

7 (4)

7 (4)

Number in cluster
19952004
(pediatric)

100% Mexico-born

53% Mexico-born

45% Mexico- born

67% Mexican assoc.

78% Mexico-born

75% US-born

96% US-born

40% Mexico- born

40% Mexico- born

100% Vietnamese assoc.

100% Vietnamese assoc.

Cluster
composition

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Patients without a source case who were clustered

None

Possible, geographic

Possible, bus routes

Possible, homeless

Possible, geographic

HH & friends

Relatives & friends

HH & friends

HH & friends

HH & relatives

HH & relatives

Epi Links within

cluster

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Table 3
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