The Biologist
(Lima)
The Biologist (Lima), 2021, vol. 19 (1), 97-103.
ORIGINAL ARTICLE / ARTÍCULO ORIGINAL
1 School of Medicine, Faculties of Health Science, Universidad Norbert Wiener, Lima, Peru
2 Hospital Nacional Docente Madre Niño San Bartolomé, Lima, Peru
3 Faculties of Medical Technology, Universidad de Chiclayo, Chiclayo, Peru
*Corresponding author: jeel.moyasalazar@icloud.pe
1,2, 3
Jeel Moya-Salazar * & Sandy Diaz
ABSTRACT
Keywords: Climate change – Diarrhea – El Nino-Southern Oscillation – Floods – Water-borne disease
Several countries are extremely susceptible to climate change and the El Niño phenomenon affecting
more than two million people in Ecuador, Colombia, and Peru. We aimed to evaluate the microbiological
quality of stagnant waters in Lambayeque region, Peru during the lockdown caused by El Niño
phenomenon. We conducted a cross-sectional study performed in the four Lambayeque districts:
(downtown Chiclayo, Mocupe, San José, and Pimentel), Perú. Two simultaneous samples were taken
from each evaluation district and were transported to Laboratory for entire microbiological analysis. We
isolated the human-pathogenic parasite (Trichuris trichiura (Linnaeus, 1771) and Entamoeba histolytica
Schaudinn, 1903), and bacteria (Staphylococcus aureus Rosenbach 1884 and Salmonella typhi
(Schroeter, 1886)) that showed patterns of resistance to conventional first-line antimicrobials (penicillin,
nalidixic acid, nitrofurantoin, and chloramphenicol). Likewise, we showed evidence of microorganisms
related to the sampling site (district) and with a degree of affectation by the phenomenon. Our result
suggests that the stagnant waters of four districts of Lambayeque presented Human-pathogenic parasites
and bacteria of high-medical importance related to the sudden changes in the climate through El Niño.
The Biologist (Lima)
ISSN Versión Impresa 1816-0719
ISSN Versión en linea 1994-9073 ISSN Versión CD ROM 1994-9081
doi:10.24039/rtb2021191886
97
HUMAN-PATHOGENIC PARASITES AND BACTERIA IN STAGNANT-WATER DURING EL NIÑO-
COSTERO PHENOMENON IN PERU
BACTERIAS Y PARÁSITOS PATÓGENOS HUMANOS AISLADOS DE AGUAS ESTANCADAS
DURANTE EL FENÓMENO EL NIÑO-COSTERO EN PERÚ
https://orcid.org/0000-0002-7357-4940
D
The Biologist (Lima). Vol. 19, Nº1, jan - jun 2021
INTRODUCTION
98
Several countries are extremely susceptible to
climate change, a phenomenon that not only has
been causing irretrievable changes in our
biodiversity but is changing the patterns of diseases
affecting human health (Metcalf et al., 2017). The
greatest consequences for infectious diseases
caused by climate change are the rapid changes in
their transmission nowadays (Greenspan et al.,
2017).
Asia-Pacific and Africa countries are affected by El
Niño phenomenon that causes extreme events
(persistent heavy rain, floods, etc.) which results in
a large number of victims, poverty, inequality, and
diseases (Glantz, 2001). In 2017, Peru was affected
by intense rains, floods, and high-daily dry
temperatures (100.4±4 ºF), which has shaped an
unusual phenomenon called El Niño-costero,
similar to El Niño phenomenon but located in the
coasts of Ecuador, Colombia, and Peru (Chinchay,
2017).
This phenomenon affected more than two million
people and had a large socioeconomic impact in
Peru, principally in the northern coastal region
(Lambayeque region). In Chiclayo, capital of the
Lambayeque region, >28000 people were affected
by the El Niño-costero phenomenon (ENCP) with
losses of infrastructure, agriculture, social and
health problems (mainly respiratory diseases and
vector and water-borne disease)(WHO, 2016).
As this phenomenon caused a stagnation of water,
stagnant waters were used as a source of human
consumption for several months. The health
consequences of the stagnation of water have not
been evaluated during ENCP, but in several
previous studies the potential risk of these for
human health is underlined (Chen et al., 2013;
Aghajani et al., 2016).
We evaluate the microbiological quality of
stagnant waters in Lambayeque region, during the
ENCP, focused on the isolation of microorganisms
of medical importance that represent a risk for the
communities exposed to these stagnant waters.
Geographic location
This descriptive study was carried out in four main
districts of Lambayeque region (27 meters-above-
sea-level,) northwest of Peru (Figure 1). Chiclayo
had ~843 445 inhabitants and is divided into eight
urban districts.
RESUMEN
Palabras clave: Enfermedades transmitidas por el agua – Diarrea – Cambio climático –Inundaciones – Fenómeno de El Niño
Varios países son extremadamente susceptibles al cambio climático y el fenómeno El Niño-costero afectó
a más de dos millones de personas en Ecuador, Colombia y Perú. Nuestro objetivo fue evaluar la calidad
microbiológica de las aguas estancadas en la región de Lambayeque, Perú, durante el estado de
emergencia causado por el fenómeno El Niño-costero mediante un estudio transversal realizado en cuatro
distritos de Lambayeque: (Centro de Chiclayo, Mocupe, San José y Pimentel), Perú. Se tomaron dos
muestras simultáneas de cada distrito de evaluación, y se trasladaron a Lima para su análisis
microbiológico completo. Aislamos parásitos patógenos humanos (Trichuris trichiura (Linnaeus, 1771) y
Entamoeba histolytica Schaudinn, 1903) y bacterias (Staphylococcus aureus Rosenbach, 1884 y
Salmonella typhi (Schroeter, 1886)) que presentaban patrones de resistencia a los antimicrobianos
convencionales de primera línea (penicilina, ácido nalidíxico, nitrofurantoína y cloranfenicol).
Asimismo, mostramos evidencia de microorganismos relacionados con el sitio de muestreo (distrito) y
con el grado de afectación por el fenómeno. Nuestro resultado sugiere que las aguas estancadas de cuatro
distritos de Lambayeque presentaron parásitos patógenos humanos y bacterias de alta importancia médica
por los cambios repentinos en el clima a través del fenómeno El Niño-costero.
MATERIAL AND METHODS
Moya-Salazar& Diaz
99
The Chiclayo's downtown has a hospital (Hospital
Regional Docente Las Mercedes -Level II), 14
health centers and six health stands, all belonging
to the Ministry of Health of Peru. Moreover, the
city has a Hospital Level I (Naylamp Hospital) and
a Level IV (Almanzor Aguinaga Asenjo Hospital)
belonging to Social Security. The ENCP affected
this region between January to May 2017, with
February being the most affected (an approximate
of 5 363 collapsed houses, and 4 595 families
affected).
Samples
The sampling was performed in the four
DISCUSIÓN Lambayque's districts: two zones of Mocupe
district (north of Chiclayo, semi-urban district of
Lagunas, >10 thousand inhabitants), the
metropolitan area of Chiclayo (downtown, >550
thousand inhabitants), San José district (west of
Chiclayo, >15 thousand inhabitants), and Pimentel
district (west of Chiclayo, >35 thousand
inhabitants). These districts were the most affected
by the phenomena keeping the waters stagnant for
≥4 weeks. We have collected randomly 4±1 ml of
samples of stagnant water from these districts
during the afternoon, after the rain, with protection
barriers.
Two simultaneous samples were taken from each
evaluation area in sterile plastic bottles of 10 ml.
The samples were stored under refrigeration (2 ±
Figure 1. Geographic distribution of the districts evaluated in the Lambayeque region, Peru.
The Biologist (Lima). Vol. 19, Nº1, jan - jun 2021
Human-pathogenic parasites and bacteria in stagnant-water
100
1ºC) for ≤5 hours until transport (~8 hours) to the
Hospital Nacional Docente Madre Niño San
Bartolome (HONADOMANI SB) in Lima. To
avoid errors in this phase, part of the sample was
transported with the BBL Culture Swab™ Plus
collection and transport system (BD, Le Pont de
Claix, France).
Microbiological analysis
All the samples were processed once they arrived at
HONADOMANI SB. The isolation were
performed following bacteriological methods in
the stool-culture area in 5% blood-sheep agar with
membrane filter grid GN-6 Metricel® 0,45μm,
47mm (PALL, NY, USA); in Karmali agar,
McConkey agar, Salmonella-Shigella agar,
Thiosulfate-Citrate-Bile-Sucrose agar, Sorbitol-
MacConkey agar, and Mannitol salt agar (all from
Merck, Darmstadt, Germany). Likewise, we used
cetrimide agar (Britania, CABA, Argentina) and
Saboraund-dextrose agar (Oxoid, Hampshire,
England).
For identification of bacteria the biochemical
®
analysis was performed with the system Vitek 2
Compact (BioMérieux, Marcy-l'Étoile, France),
and antibiogram was by disc diffusion with
Breakpoints from CLSI M100S (CLSI, 2016).The
sample was referred to the parasitology area for
identification of human-pathogenic parasites
following a previous concentration methods
(Zarlenga & Trout, 2004), included bright-field
microscopy and rapid test (rbiopharm, Darmstadt,
Germany) for most frequently parasite as amoebas
and helminths. Also, we conducted a determination
of Rotavirus (Rota-Strip, Coris Bioconcept,
Gembloux, Belgium). The microbial enumeration
techniques employed in this research were the
Most Probable Number (MPN) techniques
following the previous protocol (Leuta, 2015).
Opportunistic bacteria of non-fecal origin were not
evaluated.
Statistical analysis
The MPN was estimated by the number of positive
tubes for coliforms in each dilution. The Spearman
correlation and T-student non-paired test analysis
was performed to show the difference between the
samples analyzed and isolations considering a p-
value <0.05 was considered statistically
significant. The statistical analysis was done by
IBM SPSS v21.0 (Armonk, USA).
Ethical aspects
This study was approved by the Research
Committee of the University of Chiclayo (Officio
Nº102-2017). In addition, this study was approved
by the HONADOMANI SB Ethics and Research
Committee (Exp. Nº 16913-16).
Pimentel's district was the most affected and
Chiclayo was the least affected. Ten samples [four
(40%) samples from Mocupe district, and two
samples (20%) from San José, Chiclayo, and
Pimentel each] were included in this study. Of the
20 analyzes (10 with the transport-medium system
and ten directly from water samples), in 6 (30%)
and 2 (10%) were isolated Enterobacterias
(Salmonella typhi (Schroeter, 1886) and
Plesiomona shigelloides (Bader, 1954) Habs &
Schubert, 1962), and Staphylococcus aureus
Rosenbach, 1884 (both ≥100 000 UFC).
Escherichia coli (Escherich, 1885) were not
isolated and rotavirus was not evident in stagnant
water samples. Differences were found between
the sampling sites (districts), and isolates of
pathogenic bacteria (t=-2.70, p = 0.001).
We reported S. aureus beta-lactam (penicillin)
resistant and sensitivity to methicillin (SAMS),
also S. typhi were resistant to nitrofurans
(nitrofurantoin), anfenicoles (chloramphenicol),
and quinolones (nalidixic acid).
6
The highest faecal coliform count was 5.1 × 10
microorganisms/100 ml obtained in Pimentel
district, and the average faecal coliform count was
6
4.4 ± 0,7×10 microorganisms/100mL in all the
sampling sites. The MPN counts ranged between
4
4.9 × 10 microorganisms/100mL (lowest)
8
recorded at Chiclayo district and 1.9 × 10
microorganisms/100mL (highest) detected at
Pimentel district. Both faecal coliform count and
MNP exceeded the acceptable limits.
As for parasitological findings, only in the
Pimentel district was found eggs of Trichuris
trichiura (Linnaeus, 1771) (human whipworm)
and two trophozoites of the protozoa Entamoeba
histolytica Schaudinn, 1903 (Figure 2).
RESULTS
The Biologist (Lima). Vol. 19, Nº1, jan - jun 2021
Moya-Salazar& Diaz
101
The Pimentel district showed the greatest bacterial
and parasitic contamination (50%). A significant
positive correlation was found between the
parasitological findings and the place of origin of
the samples (rho=0.52, p = 0.002). No difference
was found in the microbiological analysis between
samples (t= -0.38, p = 0.74), nor between the
findings in the transport-medium system and from
water samples (t= -2.95, p = 0.001).
We demonstrated for the first time the isolation of
pathogenic microorganisms of high medical
importance that showed patterns of resistance to
conventional first-line antimicrobials. Our results
also showed evidence of parasites related to the
sampling site (district) and the level of effects by
the ENCP at Lambayeque, Peru.
DISCUSIÓN
Climate change is not only changing the dynamics
of infections, but it is also threatening public and
planetary health. From these changes, economic
opportunities arise but also natural phenomena that
bring with them changes in the parasite-host
relationship. These changes have been accentuated
on the coast at the marine, protozoic and bacterial
level (Bradley et al., 2005; Byers et al., 2020). The
findings found in this study are consistent with
previous studies that place human pathogens as
emergent related to climate change phenomena
(Ryan et al., 2019; El-Sayed & Kamel, 2020). It is
necessary in Peru, a country with a high prevalence
of infectious diseases and vulnerable to climate
change, that continuous monitoring of emergencies
and re-emergencies of infectious diseases
associated with climatic phenomena be developed
in order to prevent and mitigate their consequences
for health and environmental (Ogden, 2018).
The ENCP caused that most of water (potable and
Figure 2. Typical views of the district areas evaluated in Lambayeque, Peru, and the parasitological finds in Pimentel district. A.
San Jose district under stagnant water, B. water stagnation conditions for two weeks in Chiclayo downtown near one of the health
centers (left), C. Many of the streets of the Pimentel district are unpaved and the heavy rains and floods caused by El Niño-costero
phenomenon resulted in stagnation of water on stilts. Even in this image you can see a group of children swimming in these waters
(white narrow). D. the nematode Trichuris trichiura (40x) found in the samples of Pimentel district.
The Biologist (Lima). Vol. 19, Nº1, jan - jun 2021
Human-pathogenic parasites and bacteria in stagnant-water
Aghajani, A.; Dabirzadeh, M.; Maroufi, Y. &
Hooshyar, H. 2016. Identification of
Acanthamoeba genotypes in pools and
stagnant water in ponds in Sistan Region in
Southeast Iran. Türkiye Parazitoloji
Dergisi, 40:132-136.
Ashbolt, N.J. 2004. Microbial contamination of
drinking water and disease outcomes in
developing regions. Toxicology, 198:
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Bradley, M.J.; Kutz, S.J.; Jenkins, E. & O'Hara,
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areas were analyzed and our results may be
restricted to the analyzed areas, ii) due to the 2017
Peruvian lockdown we did not perform molecular
analyzes to confirm the genes associated with
bacterial resistance, iii) the present study was
developed with conventional bacteriological
methods, therefore no sequencing of the analyzed
samples was used, iv) finally, we did not monitor
the areas analyzed, in order to understand the
behav io r an d c hange s i n pa th ogeni c
microorganisms.
In conclusion, this study suggests that the stagnant
waters of four districts of Lambayeque presented
Human-pathogenic parasites and bacteria of high-
medical importance that places people at high risk
of infection and development of acute diarrheal
disease.
We thank the support of all the team workers of
Pathology Department (Specially of Javier Soto,
Alfonso Terán, and Victor Rojas-Zumarán) of the
Hospital Nacional Docente Madre Niño San
Bartolome in Lima, Perú.
Funding: Self-funding by the authors
Conflict of interest: The authors declare that they
have no conflict of interest.
102
free) contains impurities and organic remains,
polluting the large numbers of water reserves, and
shortages and/or limiting access to clean water for
human consumption in the affected districts of
Lambayeque. This leads the phenomena-affected
communities to use and consume water from other
sources (such as stagnant water) under different
rudimentary water-treatment systems. Greater
6
faecal coliform (5.1 × 10 microorganisms/100
8
m L ) a n d t h e M P N ( 1 . 9 × 1 0
microorganisms/100mL) were indicative of the
low quality of stagnant water and the high risk to
which these communities are exposed. Our
findings agree with previous reports on MPN in
waters in developing countries with high frequency
of climatic phenomena (Emiliani, 2004; Venegas-
Pérez et al., 2016).
Faecal contamination of these stagnant waters may
be responsible for health-associated problems, like
the acute diarrheal disease (220 425 cases) mainly
in children (Silva & Hernández, 2017). Our data
agree and showed coliforms, Enterobacterias (S.
typhi cause of Typhoid fever, P. shigelloides related
to diarrheal and gastroenteritis) and parasites (T.
trichiura and E. hystolitica cause of persists
diarrhea) highly dangerous for human health.
The adaptation of these pathogens in stagnant
waters composes a risk mainly for children (Figure
2) . Se ver al e va l ua tio ns h av e sh own
microbiological contamination in drinking water
worldwide, highlighting high frequency and risk in
low-income countries (Ashbolt 2004; van der
Wielen & van der Kooij, 2013). Other findings
only in the district of Pimentel evidenced protozoa
and helminths on these stagnant waters. Under the
precarious conditions caused by the ENCP the
regional level four major hospitals were declared in
red alert (Vega, 2017), and the other health centers
showed flaws in basic services (due to flooding,
access obstruction (Figure 2), lack of personnel,
etc.). This deficiency of solidity in the health
system has been affected during the current
COVID-19 pandemic, under this scenario; new
prevention strategies must be included in a
framework of sustainability (Ottersen &
Engebretsen, 2020).
The results of this study should be interpreted with
the following limitations: i) Due to the limitations
of access to the sampling areas, no more sampling
ACKNOWLEDGEMENT
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Received October 29, 2020.
Accepted January 16, 2021.
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