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Introduction
I am an infectious diseases epidemiologist and lead the Emerging Infections and Climate Change Research Unit and Masters’ and Doctoral programs in Epidemiological Research at Universidad Peruana Cayetano Heredia. I also have joint appointments at the Tulane, Johns Hopkins, Wake Forest and Texas Medical Branch universities. I studied at Johns Hopkins, have published >100 scientific articles and trained thousands of post-graduate students under major capacity building efforts of regional impact.
Current institution
Publications
Publications (241)
Peccaries (collared peccary—CP—and white-lipped peccary—WLP) are an essential source of protein and income for rural communities in the Amazon region. Since 1980s, researchers in the Amazon have reported recurrent local disappearances of WLP populations. Although such disappearances impact the species conservation and the food security of rural soc...
Trachoma is targeted for global elimination as a public health problem by 2030. Measurement of IgG antibodies in children is being considered for surveillance and programmatic decision making. There are currently no guidelines for applications of serology, which represents a generalizable problem in seroepidemiology and disease elimination. We coll...
Hepatitis B virus (HBV) and Hepatitis E virus (HEV) are zoonotic pathogens posing
significant health concerns in rural Amazonia, a region marked by high endemicity, poverty, and limited healthcare access. However, the epidemiology of HBV and HEV in this ecosystem remains underexplored. This study examines the circulation of HBV and HEV at the human...
Background
Mass drug administration (MDA) with niclosamide (NSM) can be used to control taeniasis, the cause of neurocysticercosis. NSM is 84.3% effective against taeniasis and is considered safe as it is not absorbed from the intestinal tract. However, information on its safety and effectiveness during MDA is limited. We evaluated the effectivenes...
Background
Malaria remains a global health challenge, particularly in Peru's Loreto region. Despite ongoing efforts, high infection rates and asymptomatic cases perpetuate transmission. The Peruvian Ministry of Health’s “Zero Malaria Plan” targets elimination. This novel study combines microscopic, molecular, and serological techniques to assess tr...
Toxoplasma gondii is a ubiquitous zoonotic protozoan parasite that infects a wide variety range of warm-blooded animals. This study describes the epidemiological scenario of T. gondii in an indigenous community that relies on subsistence hunting in a well-conserved and isolated area of the Peruvian Amazon. The high seropositivity against T. gondii...
Background
Malaria continues to pose a significant public health challenge in the Loreto region of the Peruvian Amazon, prompting the implementation of the "Plan Malaria Cero" to minimize cases and eliminate malaria in the region. However, the need for reliable diagnostic tools to monitor changes in transmission intensity and guide interventions re...
In order to understand the impacts in the post-disaster scenario of the 2017 El Niño events in the Piura region-Peru, we examined post-traumatic stress disorder (PTSD), food insecurity (FI), and social capital (SC) across three-time points in mothers in highly affected areas. In the Piura, Castilla, and Catacaos districts, we studied mothers combin...
Introduction
Understanding human mobility’s role in malaria transmission is critical to successful control and elimination. However, common approaches to measuring mobility are ill-equipped for remote regions such as the Amazon. This study develops a network survey to quantify the effect of community connectivity and mobility on malaria transmissio...
In 2023, a series of climatological and political events unfolded, partly driving forward the global climate and health agenda while simultaneously exposing important disparities and vulnerabilities to climate-related events. On the policy front, a significant step forward was marked by the inaugural Health Day at COP28, acknowledging the profound...
Malaria parasites are known to infect a variety of vertebrate hosts, including ungulates. However, ungulates of Amazonia have not been investigated. We report for the first time, the presence of parasite lineages closely related to Plasmodium odocoilei clade 1 and clade 2 in free-ranging South American red-brocket deer (Mazama americana; 44.4%, 4/9...
Enzyme-linked immunoelectrotransfer blot (EITB) detects antibodies against seven Taenia solium larvae antigens in three protein families (GP50, T24/42, and 8-kDa) with different structures and functions. EITB banding patterns against these antigens in pigs provide information about the course of infection and may discriminate viable cysticercosis....
Objectives: Understanding human mobility's role on malaria transmission is critical to successful control and elimination. However, common approaches to measuring mobility are ill-equipped for remote regions such as the Amazon. This study develops a network survey to quantify the effect of community connectivity and mobility on malaria transmission...
Background
Rapid diagnostic testing may support improved treatment of COVID patients. Understanding COVID testing and care pathways is important for assessing the impact and cost-effectiveness of testing in the real world, yet there is limited information on these pathways in low-and-middle income countries (LMICs). We therefore undertook an expert...
South America is experiencing the effects of climate change, including extreme weather events and changes in temperature and precipitation patterns. These effects interact with existing social vulnerabilities, exacerbating their impact on the health and wellbeing of populations. This viewpoint highlights four main messages from the series, which pr...
Climate-related phenomena in Peru have been slowly but continuously changing in recent years beyond historical variability. These include sea surface temperature increases, irregular precipitation patterns and reduction of glacier-covered areas. In addition, climate scenarios show amplification in rainfall variability related to the warmer conditio...
Background: Rapid diagnostic testing may support improved treatment of COVID patients. Understanding COVID testing and care pathways is important for assessing the impact and cost-effectiveness of testing in the real world, yet there is limited information on these pathways in low-and-middle income countries (LMICs). We therefore undertook an exper...
Introduction
Worldwide, prisons are high-risk settings for the transmission of infectious diseases such as HIV. There is a need to understand the health conditions of prisoners to improve and implement timely strategies for HIV diagnosis and control. Hence, we aimed to identify factors associated with self-reported HIV (srHIV) among Peruvian inmate...
There is an important gap in regional information on climate change and health, limiting the development of science-based climate policies in South American countries. This study aims to identify the main gaps in the existing scientific literature on the impacts, exposure, and vulnerabilities of climate change on population health. A scoping review...
Background:
Anaemia is a public health problem in Peru. In the Loreto region of the Amazon, ≥50% of children may be anaemic, although insufficient information exists for rural villages.
Methods:
To generate more data about childhood anaemia in the Peruvian Amazon, haemoglobin was measured as part of a trachoma survey in 21 randomly selected vill...
Background:
Although malaria control investments worldwide have resulted in dramatic declines in transmission since 2000, progress has stalled. In the Amazon, malaria resurgence has followed withdrawal of Global Fund support of the Project for Malaria Control in Andean Border Areas (PAMAFRO). We estimate intervention-specific and spatially-explici...
[This corrects the article DOI: 10.1371/journal.pntd.0009000.].
Leishmaniasis is a disease of public importance with a complex transmission cycle. A quantitative PCR was developed by using the small subunit of the ribosomal RNA gene (SSU rRNA) as a DNA target, which is conserved in all Leishmania species. A TaqMan ® probe was designed to have a high specificity. In all, 22 out of 23 (95.7%) ticks classified as...
The Matsigenka people living traditional lifestyles in remote areas of the Amazon rely on a fish-based diet that exposes them to methylmercury (MeHg) at levels that have been associated with decreased IQ scores. In this study, the association between Hg levels and working memory was explored using the framework of the Multicomponent Model. Working...
Haemosporidians are a widespread group of blood parasites transmitted by vectors. Despite their relevance for bird conservation, few studies have been conducted in the Amazonia and even less in terrestrial wild birds. We analysed blood samples from 168 game birds, collected from 2008 to 2015 by subsistence hunters of an indigenous rural community i...
Chemical and microbiological drinking water contaminants pose risks to child health but are not often evaluated concurrently. At two consecutive visits to 96 households in Piura, Peru, we collected drinking water samples, administered health and exposure questionnaires, and collected infant stool samples. Standard methods were used to quantify heav...
Background
Deworming programs aimed at reducing morbidity and mortality from geohelminth infections are common in many countries where these infections are endemic, but data demonstrating increasing levels of resistance to albendazole and mebendazole are causes for concern. Studies to evaluate the clinical efficacy of deworming programs are critica...
This Report provides a comprehensive, objective, open, transparent, systematic, and rigorous scientific assessment of the state of the Amazon’s ecosystems, current trends, and their implications for the long-term well-being of the region, as well as opportunities and policy relevant options for conservation and sustainable development.
Nicolaou, Laura, Anne Steinberg, Rodrigo M. Carrillo-Larco, Stella Hartinger, Andres G. Lescano, and William Checkley. Living at high altitude and COVID-19 mortality in Peru. High Alt Med Biol. 00:000-000, 2022. Background: Previous studies have reported a lower severity of COVID-19 infections at higher altitudes; however, this association may be c...
It has been suggested that pets play a critical role in the maintenance of methicillin‐resistant (MR) and multidrug‐resistant (MDR) Staphylococcus spp. in the household. We examined risk factors for carriage of antimicrobial‐resistant coagulase‐positive staphylococci, with particular attention to Staphylococcus aureus and Staphylococcus pseudinterm...
Peru celebrates 200 years of independence in 2021. Over this period of independent life, and despite the turbulent socio-political scenarios, from internal armed conflict to economic crisis to political instability over the last 40 years, Peru has experienced major changes on its epidemiological and population health profile. Major advancements in...
The diagnosis of NCC depends on neuroimaging and serological confirmation. While antibody detection by enzyme-linked immunoelectrotransfer blot (EITB) fails to predict viable NCC, EITB banding patterns provide information about the host’s infection course. Adding antigen ELISA results on EITB banding patterns may improve their ability to predict or...
Background:
Both pulmonary and mental health are affected following hospitalization for COVID-19 pneumonia. Pulmonary rehabilitation therapy has demonstrated benefits in improving mental health, but no validated combined programs that include mental health have been proposed.
Objective:
This article presents the design of a trial that aimed to a...
Objective:
To determine the relationship between socioeconomic status (SES) and visual impairment (VI) or blindness in the rural Peruvian Amazon, hypothesizing that higher SES would have a protective effect on the odds of VI or blindness.
Methods:
In this cross-sectional study of 16 rural communities in the Peruvian Amazon, consenting adults age...
Background
Improvements in technology could facilitate task-shifting and ocular disease screening in rural areas.
Methods
Visual acuity (VA) was tested using a Ministry of Health 3-m VA card. Anterior segment photographs were taken using a three-dimensional printed cellphone attachment and remotely graded.
Results
Of 326 photographed eyes, 1 was...
This Report provides a comprehensive, objective, open, transparent, systematic, and rigorous scientific assessment of the state of the Amazon’s ecosystems, current trends, and their implications for the long-term well-being of the region, as well as opportunities and policy relevant options for conservation and sustainable development.
Los bosques Amazónicos y los ecosistemas acuáticos son la base de varios servicios ecosistémicos, los cuales desempeñan un papel crucial en los medios de vida, bienestar y salud de los seres humanos. Algunos de los problemas de salud más relevantes y desafiantes de la Amazonía están relacionados con la deforestación y la degradación de los ecosiste...
We conducted a retrospective cross-sectional study of adult hospitalized patients with confirmed tuberculous meningitis to determine the impact of the timing of treatment initiation upon mortality. Mortality of tuberculous meningitis was high and associated with delay in initiation of treatment, older age, HIV infection, and higher disease severity...
Urinary tract infections (UTIs) are a common human infection. Antibiotic resistance in extended-spectrum β-lactamase (ESBL)-producing uropathogenic E. coli (UPEC) is a major therapeutic challenge due to limited treatment alternatives. The aim was to characterize the antimicrobial resistance (AMR) and dynamics of ESBL-producing UPEC isolates from UT...
The widespread and poorly regulated use of antibiotics in animal production in low- and middle-income countries (LMICs) is increasingly associated with the emergence and dissemination of antibiotic resistance genes (ARGs) in retail animal products. Here, we compared Escherichia coli from chickens and humans with varying levels of exposure to chicke...
The Peruvian-Brazilian border is a highly endemic tegumentary leishmaniasis region in South America. The interoceanic highway is a commercial route that connects Peru and Brazil through Madre de Dios and has raised concerns about its impact on previously undisturbed areas. In order to assess leishmaniasis transmission risk along this highway, we co...
Madariaga virus (MADV) has recently been associated with severe human disease in Panama, where the closely related Venezuelan equine encephalitis virus (VEEV) also circulates. In June 2017, a fatal MADV infection was confirmed in a community of Darien Province. We conducted a cross-sectional outbreak investigation with human and mosquito collection...
Border regions have been implicated as important hot spots of malaria transmission, particularly in Latin America, where free movement rights mean that residents can cross borders using just a national ID. Additionally, rural livelihoods largely depend on short-term migrants traveling across borders via the Amazon’s river networks to work in extrac...
Background
Despite the well-known widespread effects on health of the El Niño phenomenon, there is little evidence of its psychosocial impact on historically affected communities and the ways that they respond to this cyclic environmental event. We aimed to describe the perceived effects on residents’ mental health, and the barriers to achieving ps...
Flores E, Fuhr D, Simms V, et alP22 ‘You cannot build a giant umbrella over Tumbes when El Niño comes’: a qualitative study of the perceptions of El Niño ’s impact on mental health, barriers to resilience and access to support in Tumbes, Peru’ J Epidemiol Community Health 2020;74:A55.
Background:
Diagnosis of congenital Chagas disease (CChD) in most endemic areas is based on low-sensitive microscopy at birth and 9-month IgG, which has poor adherence. We aim to evaluate the accuracy of the IgM-Shed Acute Phase Antigen (IgM-SAPA) test in the diagnosis of CChD at birth.
Methods:
Two cohort studies (training and validation cohort...
Poaching and trade of wildlife for local and international exotic pet
markets result in frequent close contact between human and non-human
primates (NHP). This forced sympatry, coupled with the phylogenetic
proximity of humans and NHPs, provides multiple new opportunities for
disease emergence. Limited information is available about the presence
of...
Background
The 1997–98 El Niño/Southern Oscillation (ENSO) was one of the most important natural disasters in 20th century Peru, associated with heavy rainfall and flooding. It affected 502 000 people, ruined 944 km of roads, and damaged 580 health centres and 956 schools. Almost a quarter of all people affected (23%) came from Piura, in the northw...
Background . Madariaga virus (MADV), has recently been associated with severe human disease in Panama, where the closely related Venezuelan equine encephalitis virus (VEEV) also circulates. In June, 2017, a fatal MADV infection was confirmed in a community of Darien province.
Methods. We conducted a cross-sectional outbreak investigation with human...
The brain drain of professionals from low- and middle-income countries (LMICs) to developed countries is well documented and partially because of the challenges faced by biomedical researchers to establish themselves back at home, after training abroad. These challenges may result in the loss of highly trained individuals from LMICs and reduce the...
Alphaviruses (Togaviridae, Alphavirus) are arthropod-borne single-stranded RNA pathogens that cause febrile and neurologic disease in much of Latin America. However, many features of Alphavirus epidemiology remain unknown. In 2011, we undertook a cross-sectional study in Nueva Esperanza, an indigenous community in the Peruvian Amazon. Here, we pres...
Background: Albendazole is the drug of choice for the treatment of parenchymal neurocysticercosis, although its efficacy is suboptimal. Plasma levels of albendazole sulfoxide (ASOX), the active metabolite of albendazole, are highly variable among patients. We hypothesized that high ASOX plasma levels during albendazole therapy may be associated wit...
Background
The parasite of the genus Leishmania causes a neglected disease known as leishmaniasis, which has different clinical aspects depending on the species that infects the person and the immune response of the patient. The objective was to determine, using molecular biology, the current circulating species of Leishmania in biopsies of differe...
The pork tapeworm, Taenia solium, is among the leading causes of preventable epilepsy in the world and is common in rural areas of developing countries where sanitation is limited and pigs have access to human feces. Prior studies in rural villages of Peru have observed clusters of T. solium cysticercosis among pigs that live near human tapeworm ca...
Objective:
To study the presence of Bartonella bacilliformis in ticks collected from two wild mammals in Madre de Dios, Peru.
Results:
A total of 110 ticks were collected. Among the 43 Amblyomma spp. extracted from the 3 Tapirus terrestris only 3 were positive for B. bacilliformis. In addition, 12 out of the 67 Rhipicephalus (Boophilus) microplu...
Mentoring is a proven path to scientific progress, but it is not a common practice in low- and middle-income countries (LMICs). Existing mentoring approaches and guidelines are geared toward high-income country settings, without considering in detail the differences in resources, culture, and structure of research systems of LMICs. To address this...
Following the Fogarty International Center-supported "Mentoring the Mentors" workshops in South America, Africa, and Asia, approaches and guidelines for mentorship at institutions within these low- and middle-income country (LMIC) contexts, appropriate for the respective regional resources and culture, were implemented. Through the presentation of...
A growing body of evidence highlights the importance of competent mentoring in academic research. We describe the development, implementation, and evaluation of four regional 2-day intensive workshops to train mid- and senior-level investigators conducting public health, clinical, and basic science research across multiple academic institutions in...
Dengue virus (DENV) affects more than 100 countries worldwide. Dengue virus infection has been increasing in the southern Peruvian Amazon city of Puerto Maldonado since 2000. We designed this study to describe the prevalence of past DENV infection and to evaluate risk factors. In 2012, we conducted a cross-sectional serosurvey and administered a kn...
Background:
Congenital Trypanosoma cruzi accounts for an estimated 22% of new cases in Latin America. However, neonatal diagnosis is challenging, as 9-month follow-up for IgG testing is poor, qPCR is not routinely performed, and micromethod misses more than 40% of congenital infections.
Methods:
Biorepository samples from new mothers and their i...
Mucosal leishmaniasis (ML) is associated with progressive tissue destruction and granuloma formation, often after a considerable period of latency from an initial cutaneous infection. We report a case of recurrent epistaxis of 3 years duration and nasopharyngeal obstruction in a woman with treated cutaneous leishmaniasis nearly 30 years before and...
Cutaneous leishmaniasis is endemic to South America where diagnosis is most commonly conducted via microscopy. Patients with suspected leishmaniasis were referred for enrollment by the Ministry of Health (MoH) in Lima, Iquitos, Puerto Maldonado, and several rural areas of Peru. A 43-question survey requesting age, gender, occupation, characterizati...
In the Peruvian North Coast (PNC), the number of Plasmodium vivax malaria cases increased steadily from 2007 to 2010 despite a significant decline in the overall number of cases in Peru during the same period. To better understand the transmission dynamics of P. vivax populations in the PNC and the neighboring Ecuadorian Amazon Basin (EAB), we stud...
Purpose:
Mental disorders are a major contributor to the global burden of disease and disability, and can be extremely costly at both individual and community level. Social capital, (SC) defined as an individual's social relationships and participation in community networks, may lower the risk of mental disorders while increasing resilience capaci...
Malaria has steadily increased in the Peruvian Amazon over the last five years. This study aimed to determine the parasite prevalence and micro-geographical heterogeneity of Plasmodium vivax parasitaemia in communities of the Peruvian Amazon. Four cross-sectional active case detection surveys were conducted between May and July 2015 in four riverin...
Background
Cutaneous leishmaniasis (CL) is an important health problem in the New World affecting civilian and military populations that are frequently exposed in endemic settings. The Peruvian region of Madre de Dios located near the border with Brazil is one of the most endemic CL regions in South America with more than 4,451 reported cases betwe...
Sand fly species collected in Madre de Dios during 2015.
(XLSX)
Minimum infection rates of positive sand flies.
(XLSX)
Sand fly species collected in Madre de Dios during 2014.
(XLSX)
Positive sand fly tools for Leishmania by kDNA and Real Time PCR.
(XLSX)
We determined the prevalence rate and risk of infection of Trypanosoma cruzi and other trypanosomatids in Peruvian non-human primates (NHPs) in the wild (n = 126) and in different captive conditions (n = 183). Blood samples were collected on filter paper, FTA cards, or EDTA tubes and tested using a nested PCR protocol targeting the 24Sα rRNA gene....
Background:
The enzyme-linked immunoelectrotransfer blot (EITB) assay is the reference serological test for neurocysticercosis (NCC). A positive result on EITB does not always correlate with the presence of active infections in the central nervous system (CNS), and patients with a single viable brain cyst may be EITB negative. Nonetheless, EITB an...
To better understand the ecology of Trypanosoma cruzi in the northeastern Peruvian Amazon, we evaluated the prevalence of T. cruzi and other trypanosomatids in four orders of wild mammals hunted and consumed by inhabitants of three remote indigenous communities in the Peruvian Amazon. Of 300 wild mammals sampled, 115 (38.3%) were infected with tryp...
Plagiarism is a serious, yet widespread type of research misconduct, and is often neglected in developing countries. Despite its far-reaching implications, plagiarism is poorly acknowledged and discussed in the academic setting, and insufficient evidence exists in Latin America and developing countries to inform the development of preventive strate...
Hymenolepis nana, the dwarf tapeworm, is a common intestinal infection of children worldwide. We evaluated infection and risk factor data that were previously collected from 14,761 children aged 2-15 years during a large-scale program in northern Peru. We found that 1,124 of 14,761 children (7.61%) had H. nana infection, a likely underestimate give...
The Plasmodium falciparum protein, apical membrane antigen 1 forms a complex with another parasite protein, rhoptry neck protein 2, to initiate junction formation with the erythrocyte and is essential for merozoite invasion during the blood stage of infection. Consequently, apical membrane antigen 1 has been a target of vaccine development but vacc...
Importance:
Malaria is a disease caused by Plasmodium parasites that caused 214 million symptomatic cases and 438,000 deaths in 2015. Plasmodium vivax is the most widely distributed species, causing the majority of malaria infections outside sub-Saharan Africa. Whole-genome sequencing (WGS) of Plasmodium parasites from clinical samples has reveale...
The reemergence of malaria in Madre de Dios, in the southern Peruvian Amazon basin, in the last decade was accompanied by ecological, political, and socioeconomic changes related to the proliferation of illegal gold mining. We conducted a secondary analysis of passive malaria surveillance data reported by the health networks in Madre de Dios betwee...
Malaria in Peru, dominated by Plasmodium vivax, remains a public health problem. The 1990s saw newly epidemic malaria emerge, primarily in the Loreto Department in the Amazon region, including areas near to Iquitos, the capital city, but sporadic malaria transmission also occurred in the 1990s-2000s in both north-coastal Peru and the gold mining re...
Hymenolepis nana is the most common cestode infection in the world. However, limited information is available regarding its impact on affected populations. We studied the epidemiology and symptoms associated with hymenolepiasis among children 3-16 years old in 16 rural communities of the highlands of the Cusco region in Peru. Information on demogra...
The transmission dynamics of many arboviruses in the Amazon Basin region have not been fully elucidated, including the vectors and natural reservoir hosts. Identification of blood meal sources in field-caught mosquitoes could yield information for identifying potential arbovirus vertebrate hosts. We identified blood meal sources in 131 mosquitoes c...
Plasmodium vivax is a major public health burden, responsible for the majority of malaria infections outside Africa. We explored the impact of demographic history and selective pressures on the P. vivax genome by sequencing 182 clinical isolates sampled from 11 countries across the globe, using hybrid selection to overcome human DNA contamination....