Publications by authors named "David T S Hayman"

81 Publications

Gluten Induces Subtle Histological Changes in Duodenal Mucosa of Patients with Non-Coeliac Gluten Sensitivity: A Multicentre Study.

Nutrients 2022 Jun 15;14(12). Epub 2022 Jun 15.

Department of Pathology and Laboratory Medicine, Mayo Clinic, Rochester, MN 55907, USA.

Histological changes induced by gluten in the duodenal mucosa of patients with non-coeliac gluten sensitivity (NCGS) are poorly defined. To evaluate the structural and inflammatory features of NCGS compared to controls and coeliac disease (CeD) with milder enteropathy (Marsh I-II). Well-oriented biopsies of 262 control cases with normal gastroscopy and histologic findings, 261 CeD, and 175 NCGS biopsies from 9 contributing countries were examined. Villus height (VH, in μm), crypt depth (CrD, in μm), villus-to-crypt ratios (VCR), IELs (intraepithelial lymphocytes/100 enterocytes), and other relevant histological, serologic, and demographic parameters were quantified. The median VH in NCGS was significantly shorter (600, IQR: 400-705) than controls (900, IQR: 667-1112) ( < 0.001). NCGS patients with Marsh I-II had similar VH and VCR to CeD [465 µm (IQR: 390-620) vs. 427 µm (IQR: 348-569, = 0·176)]. The VCR in NCGS with Marsh 0 was lower than controls ( < 0.001). The median IEL in NCGS with Marsh 0 was higher than controls (23.0 vs. 13.7, < 0.001). To distinguish Marsh 0 NCGS from controls, an IEL cut-off of 14 showed 79% sensitivity and 55% specificity. IEL densities in Marsh I-II NCGS and CeD groups were similar. : NCGS duodenal mucosa exhibits distinctive changes consistent with an intestinal response to luminal antigens, even at the Marsh 0 stage of villus architecture.
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http://dx.doi.org/10.3390/nu14122487DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC9230100PMC
June 2022

Is duodenal biopsy always necessary for the diagnosis of coeliac disease in adult patients with high anti-tissue transglutaminase (TTG) antibody titres?

Frontline Gastroenterol 2022 25;13(4):287-294. Epub 2021 Jun 25.

Gastroenterology and Hepatology, Middlemore Hospital - Counties Manukau DIstrict Health Board (CMDH), Auckland, New Zealand.

Objective: Avoiding duodenal biopsy in adults for coeliac disease (CD) diagnosis is controversial. Some retrospective and prospective studies have shown that CD can be reliably diagnosed in adults with serology rather than duodenal biopsies. This study aimed to check the accuracy of a cut-off value of ≥10 upper limit of normal of anti-tissue transglutaminase antibody (anti-TTG IgA) titres for CD diagnosis in adult patients.

Method: We retrospectively analysed adult patients (≥16 years) who underwent gastroscopy from 2013 to 2018 for positive coeliac serology. The relationship between titres and disease was determined by using linear models, whereas sensitivity and specificity were assessed by receiver operator curve.

Results: We analysed 144 newly anti-TTG antibody-positive adult patients with a median age of 48.5 years (IQR 32-62); among them, 86 (60%) patients had CD (Marsh III: n=68 and Marsh II and I: n=18) with a higher prevalence in females (n=59 (69%)) and Europeans (n=60 (70%)). Fifty (58%) patients with CD had colonoscopy and five (6%) had imaging; only six patients were diagnosed with additional conditions. An anti-TTG IgA titre cut-off value of 150 U/L was 100% specific for CD in our dataset, with 70% (95% CI: 60% to 88%) sensitivity for this patient group.

Conclusion: Coeliac serology using anti-TTG IgA with titres ≥10× normal value is an excellent predictor of CD, irrespective of age, gender and ethnicity. Duodenal biopsy may not be necessary in selected adult patients with CD, especially younger than 50 years of age without additional gastrointestinal red-flag signs and symptoms.
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http://dx.doi.org/10.1136/flgastro-2020-101728DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC9186042PMC
June 2021

Present and future distribution of bat hosts of sarbecoviruses: implications for conservation and public health.

Proc Biol Sci 2022 05 25;289(1975):20220397. Epub 2022 May 25.

Massey University, Palmerston North, New Zealand.

Global changes in response to human encroachment into natural habitats and carbon emissions are driving the biodiversity extinction crisis and increasing disease emergence risk. Host distributions are one critical component to identify areas at risk of viral spillover, and bats act as reservoirs of diverse viruses. We developed a reproducible ecological niche modelling pipeline for bat hosts of SARS-like viruses (subgenus ), given that several closely related viruses have been discovered and sarbecovirus-host interactions have gained attention since SARS-CoV-2 emergence. We assessed sampling biases and modelled current distributions of bats based on climate and landscape relationships and project future scenarios for host hotspots. The most important predictors of species distributions were temperature seasonality and cave availability. We identified concentrated host hotspots in Myanmar and projected range contractions for most species by 2100. Our projections indicate hotspots will shift east in Southeast Asia in locations greater than 2°C hotter in a fossil-fuelled development future. Hotspot shifts have implications for conservation and public health, as loss of population connectivity can lead to local extinctions, and remaining hotspots may concentrate near human populations.
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http://dx.doi.org/10.1098/rspb.2022.0397DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC9130791PMC
May 2022

Uncovering the genetic diversity of Giardia intestinalis in isolates from outbreaks in New Zealand.

Infect Dis Poverty 2022 May 4;11(1):49. Epub 2022 May 4.

School of Veterinary Science, Massey University, Palmerston North, Manawatu-Wanganui, New Zealand.

Background: Giardia intestinalis is one of the most common causes of diarrhoea worldwide. Molecular techniques have greatly improved our understanding of the taxonomy and epidemiology of this parasite. Co-infection with mixed (sub-) assemblages has been reported, however, Sanger sequencing is sometimes unable to identify shared subtypes between samples involved in the same epidemiologically linked event, due to samples showing multiple dominant subtypes within the same outbreak. Here, we aimed to use a metabarcoding approach to uncover the genetic diversity within samples from sporadic and outbreak cases of giardiasis to characterise the subtype diversity, and determine if there are common sequences shared by epidemiologically linked cases that are missed by Sanger sequencing.

Methods: We built a database with 1109 unique glutamate dehydrogenase (gdh) locus sequences covering most of the assemblages of G. intestinalis and used gdh metabarcoding to analyse 16 samples from sporadic and outbreak cases of giardiasis that occurred in New Zealand between 2010 and 2018.

Results: There is considerable diversity of subtypes of G. intestinalis present in each sample. The utilisation of metabarcoding enabled the identification of shared subtypes between samples from the same outbreak. Multiple variants were identified in 13 of 16 samples, with Assemblage B variants most common, and Assemblages E and A present in mixed infections.

Conclusions: This study showed that G. intestinalis infections in humans are frequently mixed, with multiple subtypes present in each host. Shared sequences among epidemiologically linked cases not identified through Sanger sequencing were detected. Considering the variation in symptoms observed in cases of giardiasis, and the potential link between symptoms and (sub-) assemblages, the frequency of mixed infections could have implications for our understanding of host-pathogen interactions.
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http://dx.doi.org/10.1186/s40249-022-00969-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC9066983PMC
May 2022

Clinical parameters of hypervirulent Klebsiella pneumoniae disease and ivermectin treatment in New Zealand sea lion (Phocarctos hookeri) pups.

PLoS One 2022 3;17(3):e0264582. Epub 2022 Mar 3.

School of Veterinary Science, Massey University, Palmerston North, New Zealand.

Hypervirulent Klebsiella pneumoniae infection causes significant mortality of endangered New Zealand sea lion pups at Enderby Island, Auckland Islands. Gross necropsy and histopathology findings are well reported, but little is known about the clinical course of disease in affected pups. To determine factors feasible as clinical screening tools for hypervirulent K. pneumoniae in live pups, 150 pups over two field seasons (2016-18) were recruited shortly after birth for a prospective cohort study. A randomised controlled clinical treatment trial with the anthelmintic ivermectin was conducted concurrently and risk factor data and biological samples were collected approximately fortnightly. Treatment with ivermectin has been demonstrated to reduce the risk of hypervirulent K. pneumoniae mortality in pups, so effects on clinical parameters between the treated and control cohorts were also investigated. A broader sample of pups were monitored for clinical signs to investigate the course of disease in affected pups. Clinical signs, haematology and oral and rectal swabs to detect gastrointestinal carriage of hypervirulent K. pneumoniae were not useful for detection of disease prior to death. Of those pups that died due to hypervirulent K. pneumoniae, only 26.1% (18/69) had any clinical signs prior, likely a reflection of the peracute course of disease. On comparison of haematological parameters between ivermectin-treated and control pups, significantly lower total plasma protein and higher eosinophil counts were seen in control versus treated pups, however standard length as a surrogate for age was a more important influence on parameters overall than ivermectin treatment. This study also highlighted a cohort of pups with severe clinical signs suggestive of hypervirulent K. pneumoniae infection were lost to follow up at the end of the monitored season, which could be contributing to cryptic juvenile mortality.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0264582PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8893627PMC
April 2022

Transmission models indicate Ebola virus persistence in non-human primate populations is unlikely.

J R Soc Interface 2022 02 2;19(187):20210638. Epub 2022 Feb 2.

Odum School of Ecology, University of Georgia, Athens, GA 30602, USA.

Infectious diseases that kill their hosts may persist locally only if transmission is appropriately balanced by susceptible recruitment. Great apes die of Ebola virus disease (EVD) and have transmitted ebolaviruses to people. However, understanding the role that apes and other non-human primates play in maintaining ebolaviruses in Nature is hampered by a lack of data. Recent serological findings suggest that few non-human primates have antibodies to EVD-causing viruses throughout tropical Africa, suggesting low transmission rates and/or high EVD mortality (Ayouba A 2019 , 1599-1608 (doi:10.1093/infdis/jiz006); Mombo IM 2020 , 1347 (doi:10.3390/v12121347)). Here, stochastic transmission models of EVD in non-human primates assuming high case-fatality probabilities and experimentally observed or field-observed parameters did not allow viral persistence, suggesting that non-human primate populations are highly unlikely to sustain EVD-causing infection for prolonged periods. Repeated introductions led to declining population sizes, similar to field observations of apes, but not viral persistence.
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http://dx.doi.org/10.1098/rsif.2021.0638DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8820502PMC
February 2022

Genomic adaptations of Campylobacter jejuni to long-term human colonization.

Gut Pathog 2021 Dec 10;13(1):72. Epub 2021 Dec 10.

mEpiLab, Hopkirk Research Institute, Massey University, Palmerston North, 4410, New Zealand.

Background: Campylobacter is a genus of bacteria that has been isolated from the gastrointestinal tract of humans and animals, and the environments they inhabit around the world. Campylobacter adapt to new environments by changes in their gene content and expression, but little is known about how they adapt to long-term human colonization. In this study, the genomes of 31 isolates from a New Zealand patient and 22 isolates from a United Kingdom patient belonging to Campylobacter jejuni sequence type 45 (ST45) were compared with 209 ST45 genomes from other sources to identify the mechanisms by which Campylobacter adapts to long-term human colonization. In addition, the New Zealand patient had their microbiota investigated using 16S rRNA metabarcoding, and their level of inflammation and immunosuppression analyzed using biochemical tests, to determine how Campylobacter adapts to a changing gastrointestinal tract.

Results: There was some evidence that long-term colonization led to genome degradation, but more evidence that Campylobacter adapted through the accumulation of non-synonymous single nucleotide polymorphisms (SNPs) and frameshifts in genes involved in cell motility, signal transduction and the major outer membrane protein (MOMP). The New Zealand patient also displayed considerable variation in their microbiome, inflammation and immunosuppression over five months, and the Campylobacter collected from this patient could be divided into two subpopulations, the proportion of which correlated with the amount of gastrointestinal inflammation.

Conclusions: This study demonstrates how genomics, phylogenetics, 16S rRNA metabarcoding and biochemical markers can provide insight into how Campylobacter adapts to changing environments within human hosts. This study also demonstrates that long-term human colonization selects for changes in Campylobacter genes involved in cell motility, signal transduction and the MOMP; and that genetically distinct subpopulations of Campylobacter evolve to adapt to the changing gastrointestinal environment.
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http://dx.doi.org/10.1186/s13099-021-00469-7DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8665580PMC
December 2021

Community health and human-animal contacts on the edges of Bwindi Impenetrable National Park, Uganda.

PLoS One 2021 24;16(11):e0254467. Epub 2021 Nov 24.

Molecular Epidemiology and Public Health Laboratory, Hopkirk Research Institute, Massey University, Palmerston North, New Zealand.

Cross-species transmission of pathogens is intimately linked to human and environmental health. With limited healthcare and challenging living conditions, people living in poverty may be particularly susceptible to endemic and emerging diseases. Similarly, wildlife is impacted by human influences, including pathogen sharing, especially for species in close contact with people and domesticated animals. Here we investigate human and animal contacts and human health in a community living around the Bwindi Impenetrable National Park (BINP), Uganda. We used contact and health survey data to identify opportunities for cross-species pathogen transmission, focusing mostly on people and the endangered mountain gorilla. We conducted a survey with background questions and self-reported diaries to investigate 100 participants' health, such as symptoms and behaviours, and contact patterns, including direct contacts and sightings over a week. Contacts were revealed through networks, including humans, domestic, peri-domestic, and wild animal groups for 1) contacts seen in the week of background questionnaire completion, and 2) contacts seen during the diary week. Participants frequently felt unwell during the study, reporting from one to 10 disease symptoms at different intensity levels, with severe symptoms comprising 6.4% of the diary records and tiredness and headaches the most common symptoms. After human-human contacts, direct contact with livestock and peri-domestic animals were the most common. The contact networks were moderately connected and revealed a preference in contacts within the same taxon and within their taxa groups. Sightings of wildlife were much more common than touching. However, despite contact with wildlife being the rarest of all contact types, one direct contact with a gorilla with a timeline including concerning participant health symptoms was reported. When considering all interaction types, gorillas mostly exhibited intra-species contact, but were found to interact with five other species, including people and domestic animals. Our findings reveal a local human population with recurrent symptoms of illness in a location with intense exposure to factors that can increase pathogen transmission, such as direct contact with domestic and wild animals and proximity among animal species. Despite significant biases and study limitations, the information generated here can guide future studies, such as models for disease spread and One Health interventions.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0254467PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8612581PMC
December 2021

Genomic and phenotypic comparison of two Salmonella Typhimurium strains responsible for consecutive salmonellosis outbreaks in New Zealand.

Int J Med Microbiol 2021 Oct 18;311(7):151534. Epub 2021 Aug 18.

Infectious Disease Research Centre, Hopkirk Research Institute, Massey University, Palmerston North, 4410, New Zealand; New Zealand Food Safety Science and Research Centre, Hopkirk Research Institute, Massey University, Palmerston North, 4410, New Zealand.

Salmonella enterica serovar Typhimurium DT160 was the predominant cause of notified human salmonellosis cases in New Zealand from 2000 to 2010, before it was superseded by another S. Typhimurium strain, DT56 variant (DT56v). Whole genome sequencing and phenotypic testing were used to compare 109 DT160 isolates with eight DT56v isolates from New Zealand animal and human sources. Phylogenetic analysis provided evidence that DT160 and DT56v strains were distantly related with an estimated date of common ancestor between 1769 and 1821. The strains replicated at different rates but had similar antimicrobial susceptibility profiles. Both strains were resistant to the phage expressed from the chromosome of the other strain, which may have contributed to the emergence of DT56v. DT160 contained the pSLT virulence plasmid, and the sseJ and sseK2 genes that may have contributed to the higher reported prevalence compared to DT56v. A linear pBSSB1-family plasmid was also found in one of the DT56v isolates, but there was no evidence that this plasmid affected bacterial replication or antimicrobial susceptibility. One of the DT56v isolates was also sequenced using long-read technology and found to contain an uncommon chromosome arrangement for a Typhimurium isolate. This study demonstrates how comparative genomics and phenotypic testing can help identify strain-specific elements and factors that may have influenced the emergence and supersession of bacterial strains of public health importance.
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http://dx.doi.org/10.1016/j.ijmm.2021.151534DOI Listing
October 2021

What is winter? Modeling spatial variation in bat host traits and hibernation and their implications for overwintering energetics.

Ecol Evol 2021 Sep 18;11(17):11604-11614. Epub 2021 Aug 18.

Molecular Epidemiology and Public Health Laboratory Hopkirk Research Institute Massey University Palmerston North New Zealand.

White-nose syndrome (WNS) has decimated hibernating bat populations across eastern and central North America for over a decade. Disease severity is driven by the interaction between bat characteristics, the cold-loving fungal agent, and the hibernation environment. While we further improve hibernation energetics models, we have yet to examine how spatial heterogeneity in host traits is linked to survival in this disease system. Here, we develop predictive spatial models of body mass for the little brown myotis () and reassess previous definitions of the duration of hibernation of this species. Using data from published literature, public databases, local experts, and our own fieldwork, we fit a series of generalized linear models with hypothesized abiotic drivers to create distribution-wide predictions of prehibernation body fat and hibernation duration. Our results provide improved estimations of hibernation duration and identify a scaling relationship between body mass and body fat; this relationship allows for the first continuous estimates of prehibernation body mass and fat across the species' distribution. We used these results to inform a hibernation energetic model to create spatially varying fat use estimates for . These results predict WNS mortality of populations in western North America may be comparable to the substantial die-off observed in eastern and central populations.
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http://dx.doi.org/10.1002/ece3.7641DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8427580PMC
September 2021

Estimating the age of the subfamily Orthocoronavirinae using host divergence times as calibration ages at two internal nodes.

Virology 2021 11 14;563:20-27. Epub 2021 Aug 14.

Molecular Epidemiology and Public Health Laboratory, School of Veterinary Science, Massey University, New Zealand.

Viruses of the subfamily Orthocoronavirinae can cause mild to severe disease in people, including COVID-19, MERS and SARS. Their most common natural hosts are bat and bird species, which are mostly split across four virus genera. Molecular clock analyses of orthocoronaviruses suggested the most recent common ancestor of these viruses might have emerged either around 10,000 years ago or, using models accounting for selection, many millions of years. Here, we reassess the evolutionary history of these viruses. We present time-aware phylogenetic analyses of a RNA-dependent RNA polymerase locus from 123 orthocoronaviruses isolated from birds and bats, including those in New Zealand, which were geographically isolated from other bats around 35 million years ago. We used this age, as well as the age of the avian-mammals split, to calibrate the molecular clocks, under the assumption that these ages are applicable to the analyzed viruses. We found that the time to the most recent ancestor common for all orthocoronaviruses is likely 150 or more million years, supporting clock analyses that account for selection.
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http://dx.doi.org/10.1016/j.virol.2021.08.004DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8365511PMC
November 2021

First report of novel assemblages and mixed infections of Giardia duodenalis in human isolates from New Zealand.

Acta Trop 2021 Aug 23;220:105969. Epub 2021 May 23.

Molecular Epidemiology and Public Health Laboratory, Hopkirk Research Institute, Massey University, Private Bag, 11 222, Palmerston North 4442, New Zealand.

Giardia duodenalis (syn. G. intestinalis and G. lamblia) is a protozoan parasite that cause disease (giardiasis) in humans and other animals. The pathogen is classified into eight assemblages, further divided into sub-assemblages, based on genetic divergence and host specificities. There are two zoonotic subtypes known as assemblages A and B, whilst assemblages from C to H are mainly found in domesticated animals, rodents and marine mammals. Here, we report for the first time the presence of assemblage E and sub-assemblage AIII in human isolates from the South Island in New Zealand. We identified a > 99% nucleotide similarity of assemblage E and sub-assemblage AIII with sequences of the gdh gene available in GenBank from individual human samples collected in Dunedin and Christchurch, respectively. We also performed a deep sequencing approach to assess intra-host assemblage variation. The sample from Dunedin showed evidence of mixed assemblage E and zoonotic sub-assemblage BIV. The report of two novel assemblages and mixed infections provides insights into the genetic diversity, epidemiology and transmission dynamics of Giardia duodenalis in New Zealand.
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http://dx.doi.org/10.1016/j.actatropica.2021.105969DOI Listing
August 2021

Body mass and hibernation microclimate may predict bat susceptibility to white-nose syndrome.

Ecol Evol 2021 Jan 21;11(1):506-515. Epub 2020 Dec 21.

Department of Microbiology and Immunology Montana State University Bozeman MT USA.

In multihost disease systems, differences in mortality between species may reflect variation in host physiology, morphology, and behavior. In systems where the pathogen can persist in the environment, microclimate conditions, and the adaptation of the host to these conditions, may also impact mortality. White-nose syndrome (WNS) is an emerging disease of hibernating bats caused by an environmentally persistent fungus, . We assessed the effects of body mass, torpid metabolic rate, evaporative water loss, and hibernaculum temperature and water vapor deficit on predicted overwinter survival of bats infected by . We used a hibernation energetics model in an individual-based model framework to predict the probability of survival of nine bat species at eight sampling sites across North America. The model predicts time until fat exhaustion as a function of species-specific host characteristics, hibernaculum microclimate, and fungal growth. We fit a linear model to determine relationships with each variable and predicted survival and semipartial correlation coefficients to determine the major drivers in variation in bat survival. We found host body mass and hibernaculum water vapor deficit explained over half of the variation in survival with WNS across species. As previous work on the interplay between host and pathogen physiology and the environment has focused on species with narrow microclimate preferences, our view on this relationship is limited. Our results highlight some key predictors of interspecific survival among western bat species and provide a framework to assess impacts of WNS as the fungus continues to spread into western North America.
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http://dx.doi.org/10.1002/ece3.7070DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7790633PMC
January 2021

High-Yield Purification of Giardia intestinalis Cysts from Fecal Samples.

Curr Protoc Microbiol 2020 12;59(1):e117

Molecular Epidemiology and Public Health Laboratory, Hopkirk Research Institute, Massey University, Palmerston North, New Zealand.

Giardia is an enteric protozoan parasite that causes gastroenteritis in all classes of vertebrates. It is ranked among the leading causes of death in children under 5 years of age. Giardiasis affects approximately 280 million people worldwide annually, a situation exacerbated by the low availability of effective treatments and the lack of a vaccine. In addition, the parasite is difficult to manipulate in in vitro environments, which hampers the development of effective disease management strategies. This article highlights the development of a method for the purification of viable Giardia cysts from fecal samples, verified by a trypan blue dye exclusion test. This protocol produces a 10-fold increase in yield over current methods. By combining sucrose flotation with gated filtration, the protocol significantly reduces the amount of debris in the purified cysts suspension. Cyst viability is verified by a trypan blue dye exclusion test. The ability to purify large quantities of Giardia from fecal samples could advance the development of effective treatments to target this worldwide prevalent parasite. © 2020 Wiley Periodicals LLC. Basic Protocol: Purification of Giardia cysts from fecal samples Support Protocol: Cyst viability test.
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http://dx.doi.org/10.1002/cpmc.117DOI Listing
December 2020

Possibility for reverse zoonotic transmission of SARS-CoV-2 to free-ranging wildlife: A case study of bats.

PLoS Pathog 2020 09 3;16(9):e1008758. Epub 2020 Sep 3.

US Centers for Disease Control and Prevention, Atlanta, Georgia, United States of America.

The COVID-19 pandemic highlights the substantial public health, economic, and societal consequences of virus spillover from a wildlife reservoir. Widespread human transmission of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) also presents a new set of challenges when considering viral spillover from people to naïve wildlife and other animal populations. The establishment of new wildlife reservoirs for SARS-CoV-2 would further complicate public health control measures and could lead to wildlife health and conservation impacts. Given the likely bat origin of SARS-CoV-2 and related beta-coronaviruses (β-CoVs), free-ranging bats are a key group of concern for spillover from humans back to wildlife. Here, we review the diversity and natural host range of β-CoVs in bats and examine the risk of humans inadvertently infecting free-ranging bats with SARS-CoV-2. Our review of the global distribution and host range of β-CoV evolutionary lineages suggests that 40+ species of temperate-zone North American bats could be immunologically naïve and susceptible to infection by SARS-CoV-2. We highlight an urgent need to proactively connect the wellbeing of human and wildlife health during the current pandemic and to implement new tools to continue wildlife research while avoiding potentially severe health and conservation impacts of SARS-CoV-2 "spilling back" into free-ranging bat populations.
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http://dx.doi.org/10.1371/journal.ppat.1008758DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7470399PMC
September 2020

Does land use affect pathogen presence in New Zealand drinking water supplies?

Water Res 2020 Oct 27;185:116229. Epub 2020 Jul 27.

Innovative River Solutions, School of Agriculture and Environment, Massey University, Private Bag, 11 222, Palmerston North 4442, New Zealand. Electronic address:

Four microbes (Campylobacter spp., Escherichia coli, Cryptosporidium spp. and Giardia spp.) were monitored in 16 waterways that supply public drinking water for 13 New Zealand towns and cities. Over 500 samples were collected from the abstraction point at each study site every three months between 2009 and 2019. The waterways represent a range from small to large, free flowing to reservoir impoundments, draining catchments of entirely native vegetation to those dominated by pastoral agriculture. We used machine learning algorithms to explore the relative contribution of land use, catchment geology, vegetation, topography, and water quality characteristics of the catchment to determining the abundance and/or presence of each microbe. Sites on rivers draining predominantly agricultural catchments, the Waikato River, Oroua River and Waiorohi Stream had all four microbes present, often in high numbers, throughout the sampling interval. Other sites, such as the Hutt River and Big Huia Creek in Wellington which drain catchments of native vegetation, never had pathogenic microbes detected, or unsafe levels of E. coli. Boosted Regression Tree models could predict abundances and presence/absence of all four microbes with good precision using a wide range of potential environmental predictors covering land use, geology, vegetation, topography, and nutrient concentrations. Models were more accurate for protozoa than bacteria but did not differ markedly in their ability to predict abundance or presence/absence. Environmental drivers of microbe abundance or presence/absence also differed depending on whether the microbe was protozoan or bacterial. Protozoa were more prevalent in waterways with lower water quality, higher numbers of ruminants in the catchment, and in September and December. Bacteria were more abundant with higher rainfall, saturated soils, and catchments with greater than 35% of the land in agriculture. Although modern water treatment protocols will usually remove many pathogens from drinking water, several recent outbreaks of waterborne disease due to treatment failures, have highlighted the need to manage water supplies on multiple fronts. This research has identified potential catchment level variables, and thresholds, that could be better managed to reduce the potential for pathogens to enter drinking water supplies.
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http://dx.doi.org/10.1016/j.watres.2020.116229DOI Listing
October 2020

Comparative genetic diversity of species causing human infections.

Parasitology 2020 11 10;147(13):1532-1537. Epub 2020 Aug 10.

Molecular Epidemiology and Public Health Laboratory, Hopkirk Research Institute, School of Veterinary Science, Massey University, Private Bag 11 222, Palmerston North, 4442, New Zealand.

Parasites sometimes expand their host range and cause new disease aetiologies. Genetic changes can then occur due to host-specific adaptive alterations, particularly when parasites cross between evolutionarily distant hosts. Characterizing genetic variation in Cryptosporidium from humans and other animals may have important implications for understanding disease dynamics and transmission. We analyse sequences from four loci (gp60, HSP-70, COWP and actin) representing multiple Cryptosporidium species reported in humans. We predicted low genetic diversity in species that present unusual human infections due to founder events and bottlenecks. High genetic diversity was observed in isolates from humans of Cryptosporidium meleagridis, Cryptosporidium cuniculus, Cryptosporidium hominis and Cryptosporidium parvum. A deviation of expected values of neutrality using Tajima's D was observed in C. cuniculus and C. meleagridis. The high genetic diversity in C. meleagridis and C. cuniculus did not match our expectations but deviations from neutrality indicate a recent decrease in genetic variability through a population bottleneck after an expansion event. Cryptosporidium hominis was also found with a significant Tajima's D positive value likely caused by recent population expansion of unusual genotypes in humans. These insights indicate that changes in genetic diversity can help us to understand host-parasite adaptation and evolution.
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http://dx.doi.org/10.1017/S0031182020001493DOI Listing
November 2020

A large scale waterborne Campylobacteriosis outbreak, Havelock North, New Zealand.

J Infect 2020 09 29;81(3):390-395. Epub 2020 Jun 29.

Hawke's Bay District Health Board, New Zealand.

Background: We describe the investigation of a Campylobacter outbreak linked to contamination of an untreated, groundwater derived drinking water supply.

Methods: We analysed epidemiological data collected from clinician-confirmed diarrheal cases and estimated the total burden of Havelock North cases using an age-adjusted cross-sectional telephone survey. Campylobacter isolates from case fecal specimens, groundwater samples, and sheep fecal specimens from paddocks adjacent to the drinking water source were whole genome sequenced.

Findings: We estimate between 6260 and 8320 cases of illness including up to 2230 who lived outside the reticulation area, were linked to the contaminated water supply. Of these, 953 cases were physician reported, 42 were hospitalized, three developed Guillain-Barré syndrome, and Campylobacter infection contributed to at least four deaths. Of the 12 genotypes observed in cases, four were also observed in water, three were also observed in sheep and one was also observed in both water and sheep.

Interpretation: The contamination of the untreated reticulated water supply occurred following a very heavy rainfall event which caused drainage of sheep feces into a shallow aquifer. The existence of a routine clinical surveillance system for campylobacteriosis facilitated identification of the outbreak, recovery of clinical isolates, and early testing of the water for pathogens. Genotyping of the Campylobacter jejuni helped define the source of the outbreak and confirm outbreak periods and cases. Expected increases in heavy rainfall events and intensification of agriculture mean that additional safeguards are needed to protect populations from such drinking water outbreaks.

Funding: NZ Ministry of Health, Health Research Council, ESR SSIF, Royal Society.
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http://dx.doi.org/10.1016/j.jinf.2020.06.065DOI Listing
September 2020

Species and genotypes causing human cryptosporidiosis in New Zealand.

Parasitol Res 2020 Jul 3;119(7):2317-2326. Epub 2020 Jun 3.

Molecular Epidemiology and Public Health Laboratory, Hopkirk Research Institute, School of Veterinary Science, Massey University, Private Bag 11-222, Palmerston North, New Zealand.

Cryptosporidium is one of the most common causes of diarrhoea around the world. Successful management and prevention of this infectious disease requires knowledge of the diversity of species and subtypes causing human disease. We use sequence data from 2598 human faecal samples collected during an 11-year period (2009-2019) to better understand the impact of different species and subtypes on public health and to gain insights into the variation of human cryptosporidiosis in New Zealand. Human cryptosporidiosis in New Zealand is caused by a high diversity of species and subtypes. Six species cause human disease in New Zealand: C. hominis, C. parvum, C. cuniculus, C. erinacei, C. meleagridis and C. tyzzeri. Sequence analysis of the gp60 gene identified 16 subtype families and 101 subtypes. Cryptosporidium hominis IbA10G2 and C. parvum IIaA18G3R1 were the most frequent causes of human cryptosporidiosis with 27% and 29% of infections, respectively. Cryptosporidium hominis presented a peak of notified human cases during autumn (March-May) whereas most cases of human cryptosporidiosis caused by C. parvum are found during the calving and lambing season in spring (September-November). We also reported some subtypes that have been rarely detected in other countries such as IbA20G2 and IIoA13G1 and a low prevalence of the hypertransmissible and virulent IIaA15G2R1. This study provides insight into the variability of cryptosporidiosis in New Zealand essential for disease management and surveillance to prevent the introduction or spread of new species and subtypes in the country.
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http://dx.doi.org/10.1007/s00436-020-06729-wDOI Listing
July 2020

Micromanipulation System for Isolating a Single Oocyst.

Micromachines (Basel) 2019 Dec 18;11(1). Epub 2019 Dec 18.

Department of Mechanical and Electrical Engineering, Massey University, Palmerston North 4410, New Zealand.

In this paper, an integrated system for contact micromanipulation of oocysts is presented. The system integrates five actuators and a partially automated control system and contacts the oocyst using a drawn glass end effector with tip dimensions of 1 μ m. The system is intended to allow single cell analysis (SCA) of -a very harmful parasite found in water supplies-by isolating the parasite oocyst of 5 μ m diameter in a new environment. By allowing this form of analysis, the source of can be found and potential harm to humans can be reduced. The system must overcome the challenges of locating the oocysts and end effector in 3D space and contact adhesion forces between them, which are prominent over inertial forces on this scale. An automated alignment method is presented, using the Prewitt operator to give feedback on the level of focus and this system is tested, demonstrating alignment accuracy of <2 μ m. Moreover, to overcome the challenge of adhesion forces, use of dry and liquid environments are investigated and a strategy is developed to capture the oocyst in the dry environment and release in the liquid environment. An experiment is conducted on the reliability of the system for isolating a oocyst from its culture, demonstrating a success rate of 98%.
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http://dx.doi.org/10.3390/mi11010003DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7019727PMC
December 2019

Pup mortality in New Zealand sea lions (Phocarctos hookeri) at Enderby Island, Auckland Islands, 2013-18.

PLoS One 2019 21;14(11):e0225461. Epub 2019 Nov 21.

School of Veterinary Science, Massey University, Palmerston North, New Zealand.

New Zealand sea lions (Phocarctos hookeri) are an endemic and endangered species. Pup mortality at Enderby Island (50.5°S, 166.28°E) in the New Zealand sub-Antarctic has been well studied, with subsequent investigations yielding more intricate detail of the causes of mortality, as new diagnostic methods become available. Klebsiella pneumoniae was first reported in 2001-02 at this site, causing a pup mortality epizootic and is now known to be present at several colonies. This bacterium is a common mucosal commensal of humans and animals, however the agent found in pups at necropsy is a hypervirulent strain, readily recognised in microbial culture as being hypermucoviscous. Infection causes septicaemia with a common syndrome of subsequent meningitis and polyarthritis. This investigation uses histopathology and microbiology, with new modalities such as matrix assisted laser desorption/ionisation-time of flight mass spectrometry to show that Klebsiella septicaemia could have historically been, and continues to be, the most important cause of pup mortality, but has been previously underrepresented due to the often cryptic presentation and sometimes peracute course of disease. Hypermucoviscous K. pneumoniae should be considered a serious threat to pup survival in the species, causing on average 60.2% of pup deaths annually at Enderby Island between 2013 and 2018, with likely more continuing mortality following pup dispersal and the cessation of the summer monitoring season. Less common causes of death included starvation (14.8%), trauma/asphyxiation (9.9%) and other infections (7%). This study forms the basis for further evaluation of risk factors for pup mortality in the species, with a view to developing active mitigation.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0225461PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6874089PMC
March 2020

Predicting Ebola virus disease risk and the role of African bat birthing.

Epidemics 2019 12 16;29:100366. Epub 2019 Nov 16.

Molecular Epidemiology and Public Health Laboratory, Hopkirk Research Institute, Massey University, Private Bag, 11 222, Palmerston North 4442, New Zealand. Electronic address:

Ebola virus disease (EVD) presents a threat to public health throughout equatorial Africa. Despite numerous 'spillover' events into humans and apes, the maintenance reservoirs and mechanism of spillover are poorly understood. Evidence suggests fruit bats play a role in both instances, yet data remain sparse and bats exhibit a wide range of life history traits. Here we pool sparse data and use a mechanistic approach to examine how birthing cycles of African fruit bats, molossid bats, and non-molossid microbats inform the spatio-temporal occurrence of EVD spillover. We create ensemble niche models to predict spatio-temporally varying bat birthing and model outbreaks as spatio-temporal Poisson point processes. We predict three distinct annual birthing patterns among African bats along a latitudinal gradient. Of the EVD spillover models tested, the best by quasi-Akaike information criterion (qAIC) and by out of sample prediction included significant African bat birth-related terms. Temporal bat birthing terms fit in the best models for both human and animal outbreaks were consistent with hypothesized viral dynamics in bat populations, but purely spatial models also performed well. Our best model predicted risk of EVD spillover at locations of the two 2018 EVD outbreaks in the Democratic Republic of the Congo was within the top 12-35% and 0.1% of all 25 × 25 km spatial cells analyzed in sub-Saharan Africa. Results suggest that sparse data can be leveraged to help understand complex systems.
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http://dx.doi.org/10.1016/j.epidem.2019.100366DOI Listing
December 2019

Spatiotemporal Dynamics of Hantavirus Cardiopulmonary Syndrome Transmission Risk in Brazil.

Viruses 2019 10 31;11(11). Epub 2019 Oct 31.

Department of Ecology, Institute of Biosciences, São Paulo State University (UNESP), Rio Claro 13506-900, Brazil.

Background: Hantavirus disease in humans is rare but frequently lethal in the Neotropics. Several abundant and widely distributed Sigmodontinae rodents are the primary hosts of and, in combination with other factors, these rodents can shape hantavirus disease. Here, we assessed the influence of host diversity, climate, social vulnerability and land use change on the risk of hantavirus disease in Brazil over 24 years.

Methods: Landscape variables (native forest, forestry, sugarcane, maize and pasture), climate (temperature and precipitation), and host biodiversity (derived through niche models) were used in spatiotemporal models, using the 5570 Brazilian municipalities as units of analysis.

Results: Amounts of native forest and sugarcane, combined with temperature, were the most important factors influencing the increase of disease risk. Population at risk (rural workers) and rodent host diversity also had a positive effect on disease risk.

Conclusions: Land use change-especially the conversion of native areas to sugarcane fields-can have a significant impact on hantavirus disease risk, likely by promoting the interaction between the people and the infected rodents. Our results demonstrate the importance of understanding the interactions between landscape change, rodent diversity, and hantavirus disease incidence, and suggest that land use policy should consider disease risk. Meanwhile, our risk map can be used to help allocate preventive measures to avoid disease.
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http://dx.doi.org/10.3390/v11111008DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6893581PMC
October 2019

Incorporating evaporative water loss into bioenergetic models of hibernation to test for relative influence of host and pathogen traits on white-nose syndrome.

PLoS One 2019 31;14(10):e0222311. Epub 2019 Oct 31.

Wildlife Conservation Society, Wildlife Health Program, Bronx, New York, United States of America.

Hibernation consists of extended durations of torpor interrupted by periodic arousals. The 'dehydration hypothesis' proposes that hibernating mammals arouse to replenish water lost through evaporation during torpor. Arousals are energetically expensive, and increased arousal frequency can alter survival throughout hibernation. Yet we lack a means to assess the effect of evaporative water loss (EWL), determined by animal physiology and hibernation microclimate, on torpor bout duration and subsequent survival. White-nose syndrome (WNS), a devastating disease impacting hibernating bats, causes increased frequency of arousals during hibernation and EWL has been hypothesized to contribute to this increased arousal frequency. WNS is caused by a fungus, which grows well in humid hibernaculum environments and damages wing tissue important for water conservation. Here, we integrated the effect of EWL on torpor expression in a hibernation energetics model, including the effects of fungal infection, to determine the link between EWL and survival. We collected field data for Myotis lucifugus, a species that experiences high mortality from WNS, to gather parameters for the model. In saturating conditions, we predicted healthy bats experience minimal mortality. Infected bats, however, suffer high fungal growth in highly saturated environments, leading to exhaustion of fat stores before spring. Our results suggest that host adaptation to humid environments leads to increased arousal frequency from infection, which drives mortality across hibernaculum conditions. Our modified hibernation model provides a tool to assess the interplay between host physiology, hibernaculum microclimate, and diseases such as WNS on winter survival.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0222311PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6822741PMC
March 2020

Hantavirus host assemblages and human disease in the Atlantic Forest.

PLoS Negl Trop Dis 2019 08 12;13(8):e0007655. Epub 2019 Aug 12.

Molecular Epidemiology and Public Health Laboratory, Infectious Disease Research Centre, Hopkirk Research Institute, Massey University, Palmerston North, New Zealand.

Several viruses from the genus Orthohantavirus are known to cause lethal disease in humans. Sigmodontinae rodents are the main hosts responsible for hantavirus transmission in the tropical forests, savannas, and wetlands of South America. These rodents can shed different hantaviruses, such as the lethal and emerging Araraquara orthohantavirus. Factors that drive variation in host populations may influence hantavirus transmission dynamics within and between populations. Landscape structure, and particularly areas with a predominance of agricultural land and forest remnants, is expected to influence the proportion of hantavirus rodent hosts in the Atlantic Forest rodent community. Here, we tested this using 283 Atlantic Forest rodent capture records and geographically weighted models that allow us to test if predictors vary spatially. We also assessed the correspondence between proportions of hantavirus hosts in rodent communities and a human vulnerability to hantavirus infection index across the entire Atlantic Forest biome. We found that hantavirus host proportions were more positively influenced by landscape diversity than by a particular habitat or agricultural matrix type. Local small mammal diversity also positively influenced known pathogenic hantavirus host proportions, indicating that a plasticity to habitat quality may be more important for these hosts than competition with native forest dwelling species. We found a consistent positive effect of sugarcane and tree plantation on the proportion of rodent hosts, whereas defaunation intensity did not correlate with the proportion of hosts of potentially pathogenic hantavirus genotypes in the community, indicating that non-defaunated areas can also be hotspots for hantavirus disease outbreaks. The spatial match between host hotspots and human disease vulnerability was 17%, while coldspots matched 20%. Overall, we discovered strong spatial and land use change influences on hantavirus hosts at the landscape level across the Atlantic Forest. Our findings suggest disease surveillance must be reinforced in the southern and southeastern regions of the biome where the highest predicted hantavirus host proportion and levels of vulnerability spatially match. Importantly, our analyses suggest there may be more complex rodent community dynamics and interactions with human disease than currently hypothesized.
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http://dx.doi.org/10.1371/journal.pntd.0007655DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6748440PMC
August 2019

What is stirring in the reservoir? Modelling mechanisms of henipavirus circulation in fruit bat hosts.

Philos Trans R Soc Lond B Biol Sci 2019 09 12;374(1782):20190021. Epub 2019 Aug 12.

Department of Veterinary Medicine, University of Cambridge, Cambridge CB3 0ES, UK.

Pathogen circulation among reservoir hosts is a precondition for zoonotic spillover. Unlike the acute, high morbidity infections typical in spillover hosts, infected reservoir hosts often exhibit low morbidity and mortality. Although it has been proposed that reservoir host infections may be persistent with recurrent episodes of shedding, direct evidence is often lacking. We construct a generalized SEIR (susceptible, exposed, infectious, recovered) framework encompassing 46 sub-models representing the full range of possible transitions among those four states of infection and immunity. We then use likelihood-based methods to fit these models to nine years of longitudinal data on henipavirus serology from a captive colony of Eidolon helvum bats in Ghana. We find that reinfection is necessary to explain observed dynamics; that acute infectious periods may be very short (hours to days); that immunity, if present, lasts about 1-2 years; and that recurring latent infection is likely. Although quantitative inference is sensitive to assumptions about serology, qualitative predictions are robust. Our novel approach helps clarify mechanisms of viral persistence and circulation in wild bats, including estimated ranges for key parameters such as the basic reproduction number and the duration of the infectious period. Our results inform how future field-based and experimental work could differentiate the processes of viral recurrence and reinfection in reservoir hosts. This article is part of the theme issue 'Dynamic and integrative approaches to understanding pathogen spillover'.
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http://dx.doi.org/10.1098/rstb.2019.0021DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6711305PMC
September 2019

Bat tolerance to viral infections.

Authors:
David T S Hayman

Nat Microbiol 2019 05;4(5):728-729

Molecular Epidemiology and Public Health Laboratory, Infectious Disease Research Centre, Hopkirk Research Institute, Massey University, Palmerston North, New Zealand.

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http://dx.doi.org/10.1038/s41564-019-0430-9DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7097803PMC
May 2019

Bats are not squirrels: Revisiting the cost of cooling in hibernating mammals.

J Therm Biol 2019 Apr 6;81:185-193. Epub 2019 Mar 6.

Department of Biological Sciences, Texas Tech University, 2901 Main St., Lubbock, TX 79409, USA.

Many species use stored energy to hibernate through periods of resource limitation. Hibernation, a physiological state characterized by depressed metabolism and body temperature, is critical to winter survival and reproduction, and therefore has been extensively quantified and modeled. Hibernation consists of alternating phases of extended periods of torpor (low body temperature, low metabolic rate), and energetically costly periodic arousals to normal body temperature. Arousals consist of multiple phases: warming, euthermia, and cooling. Warming and euthermic costs are regularly included in energetic models, but although cooling to torpid body temperature is an important phase of the torpor-arousal cycle, it is often overlooked in energetic models. When included, cooling cost is assumed to be 67% of warming cost, an assumption originally derived from a single study that measured cooling cost in ground squirrels. Since this study, the same proportional value has been assumed across a variety of hibernating species. However, no additional values have been derived. We derived a model of cooling cost from first principles and validated the model with empirical energetic measurements. We compared the assumed 67% proportional cooling cost with our model-predicted cooling cost for 53 hibernating mammals. Our results indicate that using 67% of warming cost only adequately represents cooling cost in ground squirrel-sized mammals. In smaller species, this value overestimates cooling cost and in larger species, the value underestimates cooling cost. Our model allows for the generalization of energetic costs for multiple species using species-specific physiological and morphometric parameters, and for predictions over variable environmental conditions.
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http://dx.doi.org/10.1016/j.jtherbio.2019.01.013DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7229550PMC
April 2019
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