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Received: 16 February 2022    Revised: 8 May 2022    Accepted: 9 June 2022

DOI: 10.1111/zph.12982

S H O R T C O M M U N I C AT I O N

First exploratory study of bacterial pathogens and

endosymbionts in head lice from a Mayan community in
southern Mexico

Karla Dzul-­Rosado1 | Josefina Inés Maldonado-­Borges2 | Fernando I. Puerto-­Manzano1 |

Miguel A. Lammoglia-­Villagómez3 | Ingeborg Becker4 | Sokani Sánchez-­Montes3,4

1
Laboratorio de Enfermedades
Emergentes y Reemergentes, Centro de Abstract
Investigaciones Regionales “Dr. Hideyo
Lice represent one of the most neglected group of vectors worldwide, particularly
Noguchi”, Universidad Autónoma de
Yucatán, Mérida, Mexico in Latin America. Records of bacterial agents related to head lice are non-­existent in
2
Escuela de Medicina, Universidad this region of the continent. Many of these communities often do not have adequate
Anáhuac Mayab, Mérida, Mexico
3
access to public services and/or health protection. The normalization of this condi-
Facultad de Ciencias Biológicas
y Agropecuarias, región Tuxpan, tion prevents them from manifesting discomfort, such as bites and itching, which
Universidad Veracruzana, Veracruz, further aggravates the situation, as they can be vectors of important diseases. For
Mexico
4 this reason, the aim of this work was to identify the richness of bacterial pathogens
Centro de Medicina Tropical, Unidad de
Investigación en Medicina Experimental, (Acinetobacter, Bartonella, and Rickettsia) and endosymbionts (Wolbachia) in head lice
Facultad de Medicina, Universidad
of paediatric patients from the indigenous municipality of Hoctun, Yucatan, Mexico.
Nacional Autónoma de México, Ciudad de
México, Mexico DNA extraction was performed using the QIAamp DNA Mini Kit. For the detection
of bacterial pathogens, fragments of the gltA, rpoB, and 16S rDNA genes were ampli-
Correspondence
Sokani Sánchez-­Montes, Facultad de fied. For the detection of Wolbachia, the wsp gene was amplified. Of the 28 lice ana-
Ciencias Biológicas y Agropecuarias
lysed, the presence of two genera of bacterial pathogens was detected Acinetobacter
región Tuxpan, Carretera Tuxpan Tampico
Kilómetro 7.5, Universitaria, Tuxpan de (42.9% = 12/28) and Bartonella (7.14% = 2/28). We also detected the endosymbiont
Rodríguez Cano, Veracruz C.P. 92870,
Wolbachia (71.42% = 20/28). Our results showed that DNA from three bacteria spe-
Mexico.
Email: sok10108@gmail.com cies (Acinetobacter baumannii, Bartonella quintana, and Wolbachia pipientis) was present
with frequencies ranging from 3.57% to 71.42%. This work represents the first ex-
Funding information
Kellogs; PAPIIT IG201221 ploratory study of the diversity of agents associated with head lice (Pediculus humanus
capitis) in Mexico and Latin America. Due to the findings generated in the present
study, it is important to perform surveillance of head lice populations to identify the
degree of spread of these pathogens and their impact on populations in the region.

KEYWORDS
Acinetobacter, Bartonella, head lice, Mayan community, Pediculus humanus capitis, Wolbachia

1  |  I NTRO D U C TI O N louse, PHC]), and Pthirus pubis [crab louse, PC] (Amanzougaghene,
Piolhos sugadores é o grupo de vetores mais negligenciados do mundo Fenollar, et al., 2020a). Infestation by these ectoparasites causes
Sucking lice are one of the most unattended group of vectors world- pediculosis and phthiriasis, respectively, which present dermatologi-
wide (Barbieri et al., 2021). There are two species that parasitize hu- cal manifestations related to the intense itching caused by the bite
mans –­ Pediculus humanus (with two subspecies: Pediculus humanus of these arthropods (Amanzougaghene, Mediannikov, et al., 2020b).
humanus [body louse, PHH] and Pediculus humanus capitis [head The marked vectorial capacity of PHH for the transmission of

Zoonoses Public Health. 2022;69:729–736. wileyonlinelibrary.com/journal/zph |

© 2022 Wiley-VCH GmbH.     729
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730      DZUL-­ROSADO et al.
bacterial agents that historically have been of great relevance to
public health, such as Rickettsia prowazekii and Bartonella quintana
which are the causal agents of epidemic typhus and trench fever, is
also recognized (Fournier et al., 2002; Houhamdi et al., 2005; Burns
et al., 2014; Barbieri et al., 2021).
Recently, in the American continent, the identification of R.
prowazekii and B. quintana in PHH was carried out in Colombia,
Mexico, and Peru (Roux & Raoult, 1999; Alcántara et al., 2009;
Faccini-­Martínez et al., 2017). Yet, previous studies showed the
presence of B. quintana in PHC recovered from paediatric patients
across several rural areas of the United States and Nepal (Sasaki
et al., 2006; Eremeeva et al., 2017), as well as the detection of the
emerging Acinetobacter baumannii in France (Bouvresse et al., 2011;
Mokhtar et al., 2020).
voltados
However, studies aimed at the identification of microbial agents
in PHC in Latin America are practically non-­existent even though pe-
diculosis in children is the main health problem (Jamani et al., 2019).
Intradomiciliary transmission is high due to the fact that most of the
family members share fomites (Burkhart & Burkhart, 2007). Human
pediculosis is endemic in some populations of the state of Yucatan,
located in the northern part of the Yucatan Peninsula, Mexico
(Manrique-­Saide et al., 2011; Ponce-­Garcia et al., 2017), where it is
associated with overcrowding, and the custom of women to wear
long hair (Ortega-­Marin et al., 2013).
além disso,
Furthermore, indigenous populations in this area often have diffi-
aumentando
culties accessing public services and/or health protection, enhancing
their vulnerability to diseases associated with these ectoparasites
(ICHIP, 1999; Taplin et al., 1991; UN, 2003). The normalization of
this condition prevents them from manifesting discomfort, such as
bites and itching, which further aggravates the situation, as they are
vectors of important diseases (Yeoh et al., 2017).
The aim of this work was to identify the presence of bacterial
pathogens (Acinetobacter, Bartonella, and Rickettsia) and endosymbi-
onts (Wolbachia) in head lice collected from children in an indigenous
community in the state of Yucatan, Mexico.
2  |  M ATE R I A L S A N D M E TH O DS
The present study was carried out from August 2014 to January
2015 in basic education schools in the community of San José
Oriente, in the municipality of Hoctun, Yucatan (Figure  1a). It was
part of a community intervention to raise awareness among the in-
habitants of this region about self-­inspection and care as measures
of prevention and control of pediculosis. Knowledge of the tradi-
tions of the people in the community was taken into account to en-
sure the continuity of health care.
Lice were collected from paediatric subjects after obtaining the
consent of their parents. The samples were taken with combs and
were fixed in 70% ethanol (Figure  1b). Each specimen was trans-
ferred to a 1.5-­ml Eppendorf® tube and macerated with a 1.5-­pellet
pestle. Then, genomic DNA was extracted using the QIAamp
DNA Mini Kit of QIAGEN (Inc.). The DNA was quantified using a
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Impacts
• Louse-­borne diseases represent one of the most ne-
glected vector-­borne diseases worldwide. Particularly
in several Latin-­American countries such as Colombia,
Peru, and Mexico.
• However, studies aimed at the identification of microbial
agents in head lice Pediculus humanus capitis (PHC) in
Latin America are practically non-­existent even though
pediculosis in children is the main health problem.
• This work provides molecular evidence of Acinetobacter
baumannii, Bartonella quintana, and Wolbachia pipien-
tis in head lice from a Mayan community in southern
Mexico City.
spectrophotometer (Nanodrop-­1000, Thermo Fisher) and adjusted
to a concentration of 500 ng.
Multiple bacterial pathogens (Acinetobacter, Anaplasma/Ehrlichia,
Bartonella, and Rickettsia) and endosymbionts (Wolbachia) were as-
sessed by amplifying the 16S rDNA, rpoB, gltA, and wsp genes, using
the primers and thermal conditions of Norman et al., 1995; Braig
et al., 1998; de Sousa et al., 2006; Murphy et al., 2017, respectively.
The reaction mixture was prepared in a final volume of 25 μl, using
12.5 μl of 2× GoTaq Green Master Mix (Promega Corporation), 2 μl
of primers (2 μM, 1 μl each), 8.5 μl nuclease-­free water, and 500 ng
DNA of each sample (2 μl).
Negative (nuclease-­free water) and positive (DNA of Anaplasma
ovis [MG733099], Bartonella vinsonii vinsonii [KT326174], Ehrlichia
canis [MH917714], Rickettsia amblyommatis [KX363842], and
Wolbachia pipientis [MT828308]) were included as controls).
Amplicons were purified and sequenced at Macrogen, Korea and the
sequences were compared to those deposited in the GenBank using
the BLAST-­n tool. Additionally, a phylogenetic reconstruction using
the maximum likelihood method in MEGA v.10 was made for louse-­
borne pathogens and endosymbionts. We selected the best nu-
cleotide substitution model using the lowest Bayesian information
criterion (BIC), also in MEGA v.10. Branch support was estimated
using 1000 non-­parametric bootstraps.
Using the program for epidemiological analysis from tabulated
data (EPIDAT 3.1), we calculated the prevalence of PHC infestation
by educational level using the Chi-­squared test. The estimated odds
ratio (OR) and 95% confidence interval for the OR were analysed
through the risk estimate of crosstabs. The level of confidence was
set at 95% and significance at p < .05.
3  |  R E S U LT S
The prevalence of pediculosis in preschool children, school chil-
dren, and adolescents from the San Jose Oriente was established,
 |

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DZUL-­ROSADO et al.       731

F I G U R E 1  Representative images of
(a) the location of San Jose Oriente, in
the municipality of Hoctun, Yucatan. The
red mark represents the sampling site.
(b). Ivory comb check (hair detangling and
styling) in a preschool girl

TA B L E 1  Prevalence of pediculosis in three educational levels of the community of San Jose Oriente, Yucatan

School level N ♀ ♂ PS (%) OR(IC) ♀ (%) ♂ (%)

Preschool 61 33 28 13 (21.31) 1.000 (−) 12 (36.36) 1 (3.57)

Primary 130 66 64 11 (8.46) 0.397 (0.188–­0.834) 11 (16.66) 0
High school 84 42 42 10 (11.90) 0.499 (0.233–­1.066) 10 (23.80) 0
Total 275 141 134 34 (12.36) 33 (23.40) 1 (0.74)

Note: Test of homogeneity between levels (χ2 = 6.724; 2 degrees of freedom; p-­value 0.034) and a linear trend estimation (χ2 = 3.018; 1 degrees of
freedom; p-­value .082).
Abbreviations: %, Prevalence; ♀, Female; ♂, Male; N, total number of students recruited; OR(IC), Odds ratio/interval confidence (95%); PS, positive
students.

with an overall prevalence of 12.36% (34/275) (Table 1). The higher a Chi-­square of 6.724 and a value of p < .05 indicates that there
prevalence of pediculosis was recorded at the preschool level with is a different risk at the different educational levels, compared to
21.31% (13/61); in contrast, the primary school level exhibited the the reference preschool level (Table  1). The linear trend estima-
lowest prevalence with 8.46% (11/130). The homogeneity test with tion with a Chi-­square of 3.018 apparently suggests that there is a
 |
732      DZUL-­ROSADO et al.
linear relationship in which the lower the educational level, the risk
of becoming infested with PHC is higher. However, the value is not
statistically significant (p > .05). In relation to gender, preschool girls
had the highest prevalence with 36.36% (12/33), followed by high
school girls with 23.8% (10/42). The girls of the three school levels
presented infestation with lice. In contrast, only one male child was
parasitized by PHC. At least one head louse per child was selected
randomly for molecular detection of bacterial pathogens and endo-
symbionts. Of the 28 lice analysed, two genera of bacterial patho-
gens were detected: Acinetobacter (42.9% =  12/28) and Bartonella
(7.14% = 2/28). In the case of members of the genus Acinetobacter,
sequences of 495 bp from the 16S rDNA gene and 237 bp from the
rpoB gene were recovered. The sequences exhibited 100% (495/495
and 237/237 bp) similarity with reference sequences of A. bauman-
nii isolated from Australia and China (GenBank Accession numbers
CP054302.1 and CP087594.1, respectively). Furthermore, two sam-
ples tested positive for the genus Bartonella, using the gltA gene,
where a complete sequence of 347 bp exhibited a 99% similarity
with B. quintana detected in France (LS483373.1). We did not find
the presence of Anaplasma, Ehrlichia, or Rickettsia DNA in any of the
analysed samples.
Finally, in the case of endosymbionts, the presence of Wolbachia
was detected in 72% (20/28) of the lice samples analysed. The se-
quences exhibited 99.66% (588/590 bp) similarity to sequences from
Wolbachia sp. detected in PHC from Canada (AY331114.1).
The Maximum Likelihood analysis confirmed the identity of the
three microorganisms, which form monophyletic groups with sup-
port values ranging between 86 and 97 with sequences of A. bau-
manii, B. quintana, and W. pipientis, respectively (Figures 2–­4).
The sequences obtained in this study were deposited in the
GenBank under the following accession numbers: OM060690,
OM108474, OM108475, and OM108476 for the 16S rDNA, rpoB,
gltA, and wsp genes of Acinetobacter, Bartonella, and Wolbachia,
respectively.
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4  |  D I S C U S S I O N
In Mexico, pediculosis has been shown that it affects up to 60% of
school children, with an average prevalence that goes from 15% to
30% (Hatam-­Nahavandi et al., 2020; Sánchez-­C asas et al., 2021).
However, in the present study, the overall prevalence of head lice
was slightly lower (12.36%). Children from the preschool group ex-
hibited the highest prevalence (21.3%). This can be influenced by
a wide range of factors, such as household size and shared use of
fomites among household members (Amanzougaghene, Fenollar,
et al., 2020a; Hatam-­Nahavandi et al., 2020). In the present study,
we identified that the girls of the three school levels exhibited a
prevalence higher than 16%; in contrast, only one preschool boy
(representing a prevalence of 3.7%) was found to be infested with
lice. A recent meta-­analysis showed that the prevalence of pedic-
ulosis among boys was lower compared to girls (7% and 19%, re-
spectively). This may be due in large part to the presence of long
hair, a risk factor that has been shown in previous studies (Ortega-­
Marin et al., 2013; Hatam-­Nahavandi et al., 2020; Sánchez-­C asas
et al., 2021).
Additionally, a previous study in Mexico identified that pedic-
ulosis affects several vulnerable groups, such as indigenous com-
munities (Ortega-­Marin et al., 2013; Laguna-­A guilar et al., 2018).
According to data from Instituto Nacional de Estadística y Geografía
[INEGI] (2020), Yucatan is the entity with the second largest indig-
enous population in Mexico (23.7%), only below Chiapas (28.2%),
and has a Mayan-­speaking population concentrated in municipali-
ties of the southern and eastern part of the state where poverty
also prevails. Pediculosis has an important psychological and social
impact on the patients and their families since they are stigmatized
as having poor hygiene and living in marginalized conditions, a mis-
conception that must be combated through health education to
avoid harming the indigenous population in Yucatan (Laguna-­A guilar
et al., 2018; Hatam-­Nahavandi et al., 2020). As far as we know, no
F I G U R E 2  Maximum-­likelihood
phylogenetic tree generated using the
Kimura two-­parameter model (K2) with
Gamma distribution (+G) and Invariant
sites (+I) with a total of 731 bp of the 16S-­
rDNA, and rpoB genes concatenated from
a few members of the genus Acinetobacter.
The diamond indicates sequences
generated in Yucatan, Mexico. Bootstrap
values higher than 50 are indicated at the
nodes (−In = −2116.724). The numbers
in parentheses are GenBank accession
numbers

DZUL-­ROSADO et al.
F I G U R E 3  Maximum-­likelihood
phylogenetic tree generated using the
Tamura three-­parameter model (T92)
with Gamma distribution (+G) for a
total of 347 bp of the gltA gene from a
few members of the genus Bartonella.
The diamond indicates sequences
generated in Yucatan, Mexico. Bootstrap
values >50% are indicated at the
nodes (−In = −1747.579). The numbers
in parentheses are GenBank accession
numbers
studies have previously been carried out to identify bacterial agents
in PHC in Mexico. In the present work, A. baumanii, an emerging
opportunistic microorganism of vital importance in the nosocomial
field, was detected. This agent has been systematically studied in
the last 20 years due to its multidrug resistance mechanisms and
its high capacity to acquire virulence and resistance genes laterally,
as well as its persistence on surfaces (Mancilla-­Rojano et al., 2020).
In Mexico, it is considered a priority agent because it can generate
high fatality in patients admitted to intensive care units (Durán-­
Manuel et al., 2021). Since the 2010s, this bacterium has been re-
corded in lice associated with the paediatric population in Europe
and Asia (Bouvresse et al., 2011; Mokhtar et al., 2020). Thus, three
species (A. baumanii, Acinetobacter radioresistensis, and Acinetobacter
schindleri) have been identified in head and body lice from Algeria,
Ethiopia, Guinea, and Thailand, with A. baumanii being the most
widely distributed (Kempf et al., 2012; Sunantaraporn et al., 2015;
Mana et al., 2017; Hammoud et al., 2021). Most of the reports show
an elevated prevalence of these agents in the lice analysed, with high
genetic diversity in the recovered sequences. Although the vectorial
capacity of the PHH to become infected with A. baumanni has been
demonstrated experimentally, no trials have been carried out with
the PHC (Houhamdi & Raoult, 2006). However, their high prevalence
denotes a potential role as possible mechanical vectors of these mi-
croorganisms (Kempf et al., 2012; Sunantaraporn et al., 2015; Mana
et al., 2017; Hammoud et al., 2021). To te best of our knowledge, this
work constitutes the first report of A. baumanii in head lice in Latin
America.
One of the samples was positive for B. quintana, the caus-
ative agent of trench fever which has been neglected for the past
decades. In Mexico, there are historical records of this bacteria,
|
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      733
mainly in vulnerable populations (Varela et al., 1954). A recent study
demonstrated the circulation of this agent in 30% of body lice of
homeless people and inmates in Mexico City (Alcántara et al., 2009).
Interestingly, neither of them exhibited a competent febrile sign as-
sociable with trench fever. Recently, in Georgia, the United States, a
high prevalence of B. quintana was demonstrated in the head lice of
the paediatric population from rural areas (Eremeeva et al., 2017). As
in the case of lice analysed in Mexico City, none of the subjects with
pediculosis presented febrile manifestations (Alcántara et al., 2009).
This suggests that there may be low virulence strains that may be
circulating in the human population. Studies carried out in Ethiopia,
France, Senegal, and the United States have shown the circulation
of Bartonella in head lice in both paediatric patients and home-
less populations (Bonilla et al., 2009; Angelakis et al., 2011; Diatta
et al., 2014; Eremeeva et al., 2017). Although experimental trials
have shown that the body louse is the vector of B. quintana, it cannot
be ruled out that populations of PHC may also support this agent.
Finally, the presence of Wolbachia, an endosymbiont that has
a metabolic and reproductive impact on the invertebrate (Kubiak
et al., 2018), was demonstrated. The presence of this bacterium has
been demonstrated in almost all groups of arthropods and nema-
todes worldwide, with lineages associated with specific groups
(Correa & Ballard, 2014). In the present study, the sequences re-
covered are grouped with those detected in various genera of lice,
mainly those of the Pediculidae and Phthiridae families (Kyei-­Poku
et al., 2005; Covacin & Barker, 2007).
Due to the findings generated in the present study, it is import-
ant to perform surveillance of PHC populations to identify the de-
gree of spread of these pathogens and their impact on populations
throughout Yucatan as well as nationwide.
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734      DZUL-­ROSADO et al.

F I G U R E 4  Maximum-­likelihood phylogenetic tree generated using the Tamura three-­parameter model (T92) with Gamma distribution
(+G) for a total of 590 bp of the wsp gene from a few lineages of the genus Wolbachia. The diamond indicates sequences generated in
Yucatan, Mexico. Bootstrap values >50% are indicated at the nodes (−In = −1692.662). The numbers in parentheses are GenBank accession
numbers

AU T H O R C O N T R I B U T I O N S DATA AVA I L A B I L I T Y S TAT E M E N T

Fieldwork: KDR, JIMB. Conceived and designed the experiments:
KDR, SSM. Performed the experiments: SSM. Analyzed the data:
KDR, SSM. Contributed reagents/materials/analysis tools: KDR,
JIMB, FIPM, MALV, IB, SSM. Wrote the paper: KDR, JIMB, FIPM,
MALV, IB, SSM.
AC K N OW L E D G E M E N T S
K. Dzul-­Rosado acknowledges W.K. Kellogg Foundation for the fund-
ing provided to develop this study. This work was also supported by
UNAM-­PAPIIT IG201221. We are very grateful to the inhabitants of
the municipality of the community of San José Oriente, Yucatán, par-
ticularly to M. en C. Rocio Laviada Delgadillo, MSP. Didier Francisco
Aké Canul, LE Carlos Iván Chi May for the facilities to carry out this
study. Also, to nursery students of Facultad de Enfermería Universidad
Autónoma de Yucatán (UADY) for their assistance in the fieldwork.
We thank MC. Javier Juárez Gabriel for his assistance in preparing the
map.
C O N FL I C T O F I N T E R E S T
The authors declare that they have no competing interests.
All data included in this study are available upon request by contact
with the corresponding author.
E T H I C A L A P P R OVA L
All procedures performed were in accordance with the ethical
standards of the institution or practice at which the studies were
conducted. This research was approved by the Research Ethics
Committee of the O'Horan Hospital, in Merida, Yucatan, México.
Project Research Number: CIE-­010-­1-­14.
ORCID
Sokani Sánchez-­Montes  https://orcid.
org/0000-0001-6316-​2187
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