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New Insights in Acanthamoeba

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A special issue of Pathogens (ISSN 2076-0817).

Deadline for manuscript submissions: closed (30 March 2022) | Viewed by 45025

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Dr. María Reyes Batlle

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Guest Editor

University Institute of Tropical Diseases and Public Health of Canary Islands. University of La Laguna
Interests: protozoa; parasites; free living amoeba; water quality; chemotherapy

Special Issue Information

Dear colleagues,

During the last few decades, Acanthamoeba have been frequently reported as a potentially pathogenic free-living protozoa. The several reports of Acanthamoeba species in soil, dust, air, snow, and aquatic environments, including ponds, swimming pools or hot tubs, contact lens solutions, hospital surroundings, etc. reveal its ubiquity. The name Acanthamoeba was coined by adding the Greek term “acanth”, which means spikes, to “amoeba”, indicating the presence of spine-like structures (now known as acanthopodia) on its surface.

It has been demonstrated that this genus is capable of causing a sight-threatening keratitis (AK), fatal granulomatous encephalitis (GAE), and cutaneous disorders. While GAE cases are mainly reported among immunocompromised patients, with few cases in immunocompetent hosts, the incidence of AK has risen over the past several decades. The misunderstanding of the pathogenesis and its pathophysiology, diagnostic delays, and problems associated with chemotherapeutic interventions enhance the importance of looking into this genus.

Based on rRNA gene sequences, the genus Acanthamoeba is divided into 22 different genotypes to date (T1 – T22). The genotype T4 has been the most commonly associated with AK, GAE, and other cutaneous infections. Although we need a more in-depth examination of why T4 isolates are most abundant in human infections, there is evidence that this capability could be due to their greater virulence and transmissibility and their reduced susceptibility to chemotherapeutic agents.

Parasite biology, genetic diversity, environmental spread, and host susceptibility, among other factors, play an important role in Acanthamoeba infections. Acanthamoeba presents two stages in its life cycle, the vegetative trophozoite phase, with a diameter of 13–23 μm, and a dormant phase called cyst, of 13–23 μm. Its use as cellular model to study differentiation mechanisms, motility and phagocytosis, bacterial pathogenesis, and evolutionary processes has led to an increase in interest in this genus.

In the ecosystem, protozoa such as Acanthamoeba influence the structure of the microbial community and enhance nutrient recycling. Moreover, Acanthamoeba is capable of acting as Trojan horse for other potential human microbes, including viral, bacterial, protist, and yeast pathogens, increasing the human health risks. However, the exact nature of symbiosis and the benefits it represents for the amoeba host are still unknown.

Therefore, in spite of the large knowledge on these protozoa, we still need to clarify some aspects related to their pathogenesis and biology or their relationships with other microorganisms, which could better explain their invasion mechanisms and prevent Acanthamoeba infections. For this Special Issue of Pathogens, we invite you to submit a review or research article related to Acanthamoeba genus. We look forward to your contribution.

Potential topics include but are not limited to:

Acanthamoeba distribution in human-related environments;
The role(s) of Acanthamoeba in the ecosystems;
New therapies on Acanthamoeba;
AK and GAE diagnosis;
Acanthamoeba as Trojan horses.

Dr. María Reyes Batlle
Guest Editor

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Keywords

Acanthamoeba
ubiquity
Acanthamoeba distribution
Acanthamoeba genotyping
genotypes
keratitis
Granulomatous Amoebic Encephalitis
Acanthamoeba diagnosis
immunocompromised
therapy
prevention
Trojan horses
endosymbiont
endocytobiont

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Published Papers (11 papers)

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Editorial

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2 pages, 218 KiB

Open AccessEditorial

New Insights in Acanthamoeba

by María Reyes-Batlle, Ines Sifaoui, Rubén L. Rodríguez-Expósito, José E. Piñero and Jacob Lorenzo-Morales

Pathogens 2022, 11(5), 609; https://doi.org/10.3390/pathogens11050609 - 23 May 2022

Cited by 6 | Viewed by 2137

Abstract

Acanthamoeba is a free-living amoeba genus able to cause severe infections, such as Granulomatous amoebic encephalitis (GAE), epithelial disorders and a sight-threatening disease called Acanthamoeba keratitis (AK) [...] Full article

(This article belongs to the Special Issue New Insights in Acanthamoeba)

Research

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14 pages, 4329 KiB

Open AccessArticle

Continuous Real-Time Motility Analysis of Acanthamoeba Reveals Sustained Movement in Absence of Nutrients

by Allison Campolo, Valerie Harris, Rhonda Walters, Elise Miller, Brian Patterson and Monica Crary

Pathogens 2021, 10(8), 995; https://doi.org/10.3390/pathogens10080995 - 6 Aug 2021

Cited by 4 | Viewed by 2147

Abstract

Acanthamoeba keratitis is a serious ocular infection which is challenging to treat and can lead to blindness. While this pathogen is ubiquitous and can contaminate contact lenses after contact with water, its habits remain elusive. Understanding this organism’s natural behavior will better inform us on how Acanthamoeba colonize contact lens care systems. Acanthamoeba trophozoites were allowed to adhere to either a glass coverslip or non-nutrient agar (NNA) within a flow cell with nutrients (Escherichia coli or an axenic culture medium (AC6)) or without nutrients (Ringer’s solution). Images were taken once every 24 s over 12 h and compiled, and videos were analyzed using ImageJ Trackmate software. Acanthamoeba maintained continuous movement for the entire 12 h period. ATCC 50370 had limited differences between conditions and surfaces throughout the experiment. Nutrient differences had a noticeable impact for ATCC 30461, where E. coli resulted in the highest total distance and speed during the early periods of the experiment but had the lowest total distance and speed by 12 h. The Ringer’s and AC6 conditions were the most similar between strains, while Acanthamoeba in the E. coli and NNA conditions demonstrated significant differences between strains (p < 0.05). These results indicate that quantifiable visual tracking of Acanthamoeba may be a novel and robust method for identifying the movement of Acanthamoeba in relation to contact lens care products. The present study indicates that Acanthamoeba can undertake sustained movement for at least 12 h with and without nutrients, on both rough and smooth surfaces, and that different strains have divergent behavior. Full article

(This article belongs to the Special Issue New Insights in Acanthamoeba)

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9 pages, 2981 KiB

Open AccessArticle

The Autofluorescence Patterns of Acanthamoeba castellanii, Pseudomonas aeruginosa and Staphylococcus aureus: Effects of Antibiotics and Tetracaine

by Hari Kumar Peguda, Saabah B. Mahbub, Tashi Doma Sherpa, Dinesh Subedi, Abbas Habibalahi, Ayad G. Anwer, Zi Gu, Mark D. P. Willcox, Ewa M. Goldys and Nicole A. Carnt

Pathogens 2021, 10(7), 894; https://doi.org/10.3390/pathogens10070894 - 14 Jul 2021

Cited by 2 | Viewed by 4201

Abstract

Acanthamoeba Keratitis (AK) can lead to substantial vision loss and morbidity among contact lens wearers. Misdiagnosis or delayed diagnosis is a major factor contributing to poor outcomes of AK. This study aimed to assess the effect of two antibiotics and one anaesthetic drug used in the diagnosis and nonspecific management of keratitis on the autofluorescence patterns of Acanthamoeba and two common bacteria that may also cause keratitis. Acanthamoeba castellanii ATCC 30868, Pseudomonas aeruginosa ATCC 9027, and Staphylococcus aureus ATCC 6538 were grown then diluted in either PBS (bacteria) or ¼ strength Ringer’s solution (Acanthamoeba) to give final concentrations of 0.1 OD at 660 nm or 10⁴ cells/mL. Cells were then treated with ciprofloxacin, tetracycline, tetracaine, or no treatment (naïve). Excitation–emission matrices (EEMs) were collected for each sample with excitation at 270–500 nm with increments in 5 nm steps and emission at 280–700 nm at 2 nm steps using a Fluoromax-4 spectrometer. The data were analysed using MATLAB software to produce smoothed color-coded images of the samples tested. Acanthamoeba exhibited a distinctive fluorescence pattern compared to bacteria. The addition of antibiotics and anaesthetic had variable effects on autofluorescence. Tetracaine altered the fluorescence of all three microorganisms, whereas tetracycline did not show any effect on the fluorescence. Ciprofloxacin produced changes to the fluorescence pattern for the bacteria, but not Acanthamoeba. Fluorescence spectroscopy was able to differentiate Acanthamoeba from P. aeruginosa and S. aureus in vitro. There is a need for further assessment of the fluorescence pattern for different strains of Acanthamoeba and bacteria. Additionally, analysis of the effects of anti-amoebic drugs on the fluorescence pattern of Acanthamoeba and bacteria would be prudent before in vivo testing of the fluorescence diagnostic approach in the animal models. Full article

(This article belongs to the Special Issue New Insights in Acanthamoeba)

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13 pages, 2581 KiB

Open AccessArticle

Silver Nanoparticles Conjugated with Contact Lens Solutions May Reduce the Risk of Acanthamoeba Keratitis

by Edyta B. Hendiger, Marcin Padzik, Inés Sifaoui, María Reyes-Batlle, Atteneri López-Arencibia, Diana Zyskowska, Marta Grodzik, Anna Pietruczuk-Padzik, Jacek Hendiger, Gabriela Olędzka, Lidia Chomicz, José E. Piñero and Jacob Lorenzo-Morales

Pathogens 2021, 10(5), 583; https://doi.org/10.3390/pathogens10050583 - 11 May 2021

Cited by 11 | Viewed by 3625

Abstract

Acanthamoeba keratitis (AK), a severe sight-threatening corneal infection, has become a significant medical problem, especially among contact lens wearers. The disease manifests as eye pain, congestion, blurred vision, lachrymation, and ring-shaped infiltrates of the cornea, and can lead to permanent blindness. Inappropriate habits of contact lens users may result in an increased risk of AK infection. The anti-amoebic efficiency of popular multipurpose contact lens solutions is insufficient to reduce this risk. An effective and non-toxic therapy against AK has not yet been developed. The prevention of AK is crucial to reduce the number of AK infections. Nanoparticles are known to be active agents against bacteria, viruses, and fungi and were also recently tested against protozoa, including Acanthamoeba spp. In our previous studies, we proved the anti-amoebic and anti-adhesive activity of silver nanoparticles against Acanthamoeba castellanii. The aim of this study is to evaluate the activity, cytotoxicity, and anti-adhesive properties of silver nanoparticles conjugated with five commonly used multipurpose contact lens solutions against the Acanthamoeba castellanii NEFF strain. The obtained results show a significant increase in anti-amoebic activity, without increasing the overall cytotoxicity, of Solo Care Aqua and Opti Free conjugated with nanoparticles. The adhesion of Acanthamoeba trophozoites to the contact lens surface is also significantly reduced. We conclude that low concentrations of silver nanoparticles can be used as an ingredient in contact lens solutions to decrease the risk of Acanthamoeba keratitis infection. Full article

(This article belongs to the Special Issue New Insights in Acanthamoeba)

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11 pages, 3097 KiB

Open AccessArticle

In Vitro Evaluation of the Combination of Melaleuca alternifolia (Tea Tree) Oil and Dimethyl Sulfoxide (DMSO) against Trophozoites and Cysts of Acanthamoeba Strains. Oxygen Consumption Rate (OCR) Assay as a Method for Drug Screening

by Tania Martín-Pérez, Irene Heredero-Bermejo, Cristina Verdú-Expósito and Jorge Pérez-Serrano

Pathogens 2021, 10(4), 491; https://doi.org/10.3390/pathogens10040491 - 19 Apr 2021

Cited by 3 | Viewed by 3335

Abstract

Ameobae belonging to the genus Acanthamoeba are responsible for the human diseases Acanthamoeba keratitis (AK) and granulomatous amoebic encephalitis (GAE). The treatment of these illnesses is hampered by the existence of a resistance stage (cysts). In an attempt to add new agents that are effective against trophozoites and cysts, tea tree oil (TTO) and dimethyl sulfoxide (DMSO), separately and in combination, were tested In Vitro against two Acanthamoeba isolates, T3 and T4 genotypes. The oxygen consumption rate (OCR) assay was used as a drug screening method, which is to some extent useful in amoebicide drug screening; however, evaluation of lethal effects may be misleading when testing products that promote encystment. Trophozoite viability analysis showed that the effectiveness of the combination of both compounds is higher than when either compound is used alone. Therefore, the TTO alone or TTO + DMSO in combination were an amoebicide, but most of the amoebicidal activity in the combination’s treatments seemed to be caused mainly by the TTO effect. In fact, DMSO alone seems to be a non-amoebicide, triggering encystment. Regarding cytotoxicity, these compounds showed toxicity in human corneal epithelial cells (HCEpiC), even at low concentrations when tested in combination. In conclusion, the use of TTO and DMSO, in combination or alone, cannot be recommended as an alternative for AK treatment until more cytotoxicity and cyst adhesion tests are performed. Full article

(This article belongs to the Special Issue New Insights in Acanthamoeba)

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25 pages, 16466 KiB

Open AccessArticle

Variables Affecting the Recovery of Acanthamoeba Trophozoites

by Monica J. Crary, Rhonda Walters, Paul Shannon and Manal M. Gabriel

Pathogens 2021, 10(2), 221; https://doi.org/10.3390/pathogens10020221 - 18 Feb 2021

Cited by 5 | Viewed by 2808

Abstract

While the results of Acanthamoeba testing have been extensively published, laboratories conducting such testing are left to develop their own methods in the absence of a standardized methodology. The wide disparity of methods has resulted in equally inconsistent reported results for contact lens care (CLC) products. This study’s objective was to determine the source of these discrepancies by evaluating basic Acanthamoeba biology and their impact on antimicrobial efficacy testing, including the ability of a recovery method to stimulate a single trophozoite to proliferate. Antimicrobial efficacy testing was conducted using well-published Acanthamoeba strains, storage conditions, and growth-based recovery methods. To identify variables that influence results, test solutions with low Acanthamoeba disinfection rates were utilized to prevent differences from being masked by high log reductions. In addition, single-cell proliferation assays were executed to understand the growth requirements to stimulate trophozoite propagation in two recovery methods. These studies indicated that both nutrient density (>10⁶ CFU) and the length of plate incubation (at least 14 days) could significantly influence the accurate recovery of trophozoites. Together, this study emphasizes the need to understand how Acanthamoeba trophozoites biology can impact test methods to create divergent results. Full article

(This article belongs to the Special Issue New Insights in Acanthamoeba)

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17 pages, 4102 KiB

Open AccessArticle

Evaluating Alternate Methods of Determining the Antimicrobial Efficacy of Contact Lens Care Products against Acanthamoeba Trophozoites

by Allison Campolo, Paul Shannon and Monica Crary

Pathogens 2021, 10(2), 126; https://doi.org/10.3390/pathogens10020126 - 27 Jan 2021

Cited by 6 | Viewed by 2323

Abstract

Acanthamoeba keratitis (AK) is a serious ocular infection caused by a ubiquitous free-living amoeba, Acanthamoeba. This infection often results in extensive corneal damage and blindness, and is notoriously difficult to cure. While Acanthamoeba is an abundant organism, AK is most associated with contact lens hygiene noncompliance and inadequate contact lens care (CLC) disinfection regimens. Thus, accurate and timely antimicrobial efficacy testing of CLC solutions is paramount. Published methods for antimicrobial efficacy testing of Acanthamoeba trophozoites requires 14 days for results. Presently, alternate and/or rapid methods for evaluating CLC products rarely demonstrate equivalent results compared to commonly-reported methods. Propidium iodide is a cellular stain that can only bind to cells with damaged outer membranes. We evaluated propidium iodide staining as an alternative method for determining the relative antimicrobial efficacy of 11 different CLC products against Acanthamoeba trophozoites. Following exposure to a CLC product, the fluorescence intensity of propidium iodide in an Acanthamoeba population demonstrated a strong correlation to the log reduction determined by established, growth-based Acanthamoeba testing used to evaluate the antimicrobial efficacy of CLC products. Thus, propidium iodide was found to be an effective rapid tool for determining cell death in Acanthamoeba trophozoites following exposure to CLC solutions. Full article

(This article belongs to the Special Issue New Insights in Acanthamoeba)

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15 pages, 3754 KiB

Open AccessArticle

hBN Nanoparticle-Assisted Rapid Thermal Cycling for the Detection of Acanthamoeba

by Abdul Khaliq Rasheed, Ruqaiyyah Siddiqui, Salma Mohammed Kabir Ahmed, Shobana Gabriel, Mohammed Zayan Jalal, Akbar John and Naveed Ahmed Khan

Pathogens 2020, 9(10), 824; https://doi.org/10.3390/pathogens9100824 - 7 Oct 2020

Cited by 8 | Viewed by 3039

Abstract

Acanthamoeba are widely distributed in the environment and are known to cause blinding keratitis and brain infections with greater than 90% mortality rate. Currently, polymerase chain reaction (PCR) is a highly sensitive and promising technique in Acanthamoeba detection. Remarkably, the rate of heating–cooling and convective heat transfer of the PCR tube is limited by low thermal conductivity of the reagents mixture. The addition of nanoparticles to the reaction has been an interesting approach that could augment the thermal conductivity of the mixture and subsequently enhance heat transfer through the PCR tube. Here, we have developed hexagonal boron nitride (hBN) nanoparticle-based PCR assay for the rapid detection of Acanthamoeba to amplify DNA from low amoeba cell density. As low as 1 × 10⁻⁴ wt % was determined as the optimum concentration of hBN nanoparticles, which increased Acanthamoeba DNA yield up to ~16%. Further, it was able to reduce PCR temperature that led to a ~2.0-fold increase in Acanthamoeba DNA yield at an improved PCR specificity at 46.2 °C low annealing temperature. hBN nanoparticles further reduced standard PCR step time by 10 min and cycles by eight; thus, enhancing Acanthamoeba detection rapidly. Enhancement of Acanthamoeba PCR DNA yield is possibly due to the high adsorption affinity of hBN nanoparticles to purine (Guanine—G) due to the higher thermal conductivity achieved in the PCR mixture due to the addition of hBN. Although further research is needed to demonstrate these findings in clinical application, we propose that the interfacial layers, Brownian motion, and percolation network contribute to the enhanced thermal conductivity effect. Full article

(This article belongs to the Special Issue New Insights in Acanthamoeba)

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Review

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11 pages, 988 KiB

Open AccessReview

Acanthamoeba Keratitis, Pathology, Diagnosis and Treatment

by Nicholas Fanselow, Nadia Sirajuddin, Xiao-Tang Yin, Andrew J. W. Huang and Patrick M. Stuart

Pathogens 2021, 10(3), 323; https://doi.org/10.3390/pathogens10030323 - 10 Mar 2021

Cited by 63 | Viewed by 8003

Abstract

Acanthamoeba keratitis is an unusual corneal infection that is recently increasing in frequency and is often contracted by contact lens wearers, someone who experienced recent eye trauma, or someone exposed to contaminated waters. Acanthamoeba survive in air, soil, dust, and water. Therefore, eye trauma and poor contact lens hygiene practices lead to the entrapment of debris and thus infection. Acanthamoeba keratitis results in severe eye pain, inflammation, and defects of the epithelium and stroma that can potentially result in vision loss if not diagnosed early and treated promptly. The disease can be diagnosed using corneal scrape/biopsy, polymerase chain reactions, impression cytology, or in vivo confocal microscopy. Once diagnosed, it is usually treated with an antimicrobial combination therapy of biguanide and aromatic diadine eye drops for several months. Advanced stages of the disease result in vision loss and the need for corneal transplants. Avoiding the risk factors and diagnosing the disease early are the most effective ways to combat Acanthamoeba keratitis. Full article

(This article belongs to the Special Issue New Insights in Acanthamoeba)

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25 pages, 1410 KiB

Open AccessReview

A Systematic Review of Intracellular Microorganisms within Acanthamoeba to Understand Potential Impact for Infection

by Binod Rayamajhee, Dinesh Subedi, Hari Kumar Peguda, Mark Duncan Willcox, Fiona L. Henriquez and Nicole Carnt

Pathogens 2021, 10(2), 225; https://doi.org/10.3390/pathogens10020225 - 18 Feb 2021

Cited by 47 | Viewed by 9446

Abstract

Acanthamoeba, an opportunistic pathogen is known to cause an infection of the cornea, central nervous system, and skin. Acanthamoeba feeds different microorganisms, including potentially pathogenic prokaryotes; some of microbes have developed ways of surviving intracellularly and this may mean that Acanthamoeba acts as incubator of important pathogens. A systematic review of the literature was performed in order to capture a comprehensive picture of the variety of microbial species identified within Acanthamoeba following the Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA) guidelines. Forty-three studies met the inclusion criteria, 26 studies (60.5%) examined environmental samples, eight (18.6%) studies examined clinical specimens, and another nine (20.9%) studies analysed both types of samples. Polymerase chain reaction (PCR) followed by gene sequencing was the most common technique used to identify the intracellular microorganisms. Important pathogenic bacteria, such as E. coli, Mycobacterium spp. and P. aeruginosa, were observed in clinical isolates of Acanthamoeba, whereas Legionella, adenovirus, mimivirus, and unidentified bacteria (Candidatus) were often identified in environmental Acanthamoeba. Increasing resistance of Acanthamoeba associated intracellular pathogens to antimicrobials is an increased risk to public health. Molecular-based future studies are needed in order to assess the microbiome residing in Acanthamoeba, as a research on the hypotheses that intracellular microbes can affect the pathogenicity of Acanthamoeba infections. Full article

(This article belongs to the Special Issue New Insights in Acanthamoeba)

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Other

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9 pages, 1103 KiB

Open AccessBrief Report

Concentrations of PGE₂ and TXB₂ in the Eyes of Mice with Disseminated Acanthamoebiasis

by Karolina Kot, Daria Kołodziej, Patrycja Kupnicka, Danuta Izabela Kosik-Bogacka and Natalia Łanocha-Arendarczyk

Pathogens 2022, 11(4), 438; https://doi.org/10.3390/pathogens11040438 - 4 Apr 2022

Cited by 2 | Viewed by 1719

Abstract

Previous studies have shown that Acanthamoeba spp. may invade the eyes by migrating along the optic nerve to the eyes from the brain. This study aimed to confirm the presence of inflammation in the eyes of mice with disseminated acanthamoebiasis by examining prostaglandin E₂ (PGE₂) and thromboxane B₂ (TXB₂) concentrations in the eyes of immunocompetent and immunocompromised mice intranasally inoculated with Acanthamoeba spp. The PGE₂ concentration was statistically significantly lower in the immunocompromised amoebae-infected mice on 8 dpi compared with the noninfected group of animals, and it was higher in the eyes of immunosuppressed amoebae-infected mice on 16 dpi than in the control group of animals. There was a statistically significant lower TXB₂ concentration in the eyes of immunocompetent infected mice compared with the noninfected group on 8 dpi. However, on 24 dpi, we noted statistically significant higher TXB₂ levels in the immunocompetent infected mice than in the control group. In immunocompromised mice, there was a lower TXB₂ level on 8 dpi than in control mice. This study confirmed the existence of an inflammatory process in the eyes of immunocompetent and immunocompromised mice infected with Acanthamoeba spp. without damaged corneas. Full article

(This article belongs to the Special Issue New Insights in Acanthamoeba)

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