Volume 45

Number 5
September 2024
 ®
Journal of Environmental Biology
p-ISSN: 0254-8704 • e-ISSN: 2394-0379 • CODEN: JEBIDP

(An International Research Journal of Environmental Sciences and Toxicology)

JEB
Editorial Board - 2024
Founder Editor-in-Chief : Dr. R. C. Dalela (1980-2022)

The Editorial Board members of Journal of Environmental Biology comprises qualified academicians from institutions
worldwide. They assist in scholarly publication of research papers in Journal of Environmental Biology.
It is hoped that the journal will achieve greater scientific excellence with their cooperation and expertise.

Executive Editor Managing Editor

Professor Divakar Dalela, M.S., M.Ch., FAMS, Mrs. Kiran Dalela
Former Head, Department of Urology, Journal of Environmental Biology
King George's Medical University, Lucknow, India Lucknow, India

Editor
Dr. Sumati Gaumat, Ph. D., Journal of Environmental Biology, Lucknow, India (Botany)

Advisory Editors
Professor S.S.S. Sarma, National Autonomous University of Mexico, Tlalnepantla, Mexico (Limnology and Eco-toxicology)
Dr. Amit Kumar Ghosh (Emeritus Scientist), Birbal Sahni Institute of Palaeosciences, Lucknow, India (Palaeobiology & Past Climatology)
Professor Em. Suresh V.S. Rana, Choudhary Charan Singh University, Meerut, India (Toxicology)
Professor Eric M. Hallerman, Virginia Polytechnic Institute and State University, Virginia, U.S.A. (Genetics & Aquaculture)
Dr. George N. Zaimes, International Hellenic University, Drama, Greece (Watershed and Riparian Areas Management & Soil Conservation)

Associate Editors
Professor Anastasia Pantera, Agricultural University of Athens, Karpenissi, Central Greece (Agroforestry & Forestry)
Professor N.K. Dubey, Banaras Hindu University, Varanasi, India (Bioprospection & Pesticides Toxicology)
Professor Surendra S. Bargali, Kumaun University, Nainital, India (Ecology)
Professor Anand Kar, Devi Ahilya University, Indore, India (Heavy Metal, Pesticide & Drug Toxicity)
Dr. K. Sadasivan Pillai, International Institute of Biotechnology and Toxicology, Padappai, India (Toxicology)
Dr. T.V. Ramachandra, Indian Institute of Science, Bengaluru, India (Aquatic Ecosystem, Biodiversity & Conservation)
Professor Sudip Barat, University of North Bengal, Siliguri, India (Fisheries, Aquaculture, Limnology & Eco-Toxicology)
Dr. A.K. Chakravarthy (Rtd.), Indian Institute of Horticultural Research, Bangalore, India (Entomology & Nematology)
Professor C.P. Srivastava, Banaras Hindu University, Varanasi, India (Agricultural Entomology)
Professor Munir Ozturk (Rtd.), Ege University, Izmir, Turkey (Eco-physicology)
Professor Mohd. Y. A. Shukor, University Putra Malaysia, Selangor, Malaysia (Environmental Biochemistry)
Dr. Qtae Jo, Hanseo University, Chungnam, Republic of Korea (Aquaculture-Environment)
Dr. Sujoy Saha, ICAR- National Research Centre for Grapes, Pune, India (Plant Pathology)
Professor Sanjay-Swami, College of Post Graduate Studies in Agricultural Sciences(CAU), Umiam, India (Natural Resource Management)
Contd......
Journal of Environmental Biology, September 2024
 ®
Journal of Environmental Biology
p-ISSN: 0254-8704 • e-ISSN: 2394-0379 • CODEN: JEBIDP JEB
Consulting Editors
Dr. Daeui Park, Korea Institute of Toxicology, Daejeon, South Korea (Toxicology)
Professor P. J. John, University of Rajasthan, Jaipur, India (Environmental Toxicology)
Professor Manjulatha Chapara, Andhra University, Visakhapatnam, India (Crustacean Physiology, Aquaculture)
Dr. Gerardo Díaz-Godínez, Autonomous University of Tlaxcala, Tlaxcala, Mexico (Fungal Biotechnology)
Dr. Saurabh Chandra, Dabur Research Foundation, Ghaziabad, India (Zoology & Animal Toxicology)
Dr. K. M. Rajesh, ICAR - Central Marine Fisheries Research Institute, Mangaluru, India (Marin Ecology, Biodiversity & Fish Biology)
Dr. Debajit Sarma, ICAR-Central Institute of Fisheries Education, Versova, India (Aquaculture)
Dr. Dharmendra Kumar Meena, ICAR-Central Inland Fisheries Research Institute, Barrackpore, India (Fisheries Resource Management)
Dr. Tapati Das, Assam University, Silchar, India (Aquatic Ecology & Biodiversity)
Dr. Santosh Kumar Karn, Sardar Bhagwan Singh University, Dehradun, India (Environmental Biotechnology)
Dr. Mukesh K Meghvansi, Defence Research & Development Establishment (DRDO), Gwalior, India (Microbial Biotechnology)
Dr. Karmabeer Jena, Central Tasar Research and Traing Institute (CSB), Ranchi, India (Biochemistry)
Professor Bharat Bhusan Patnaik, Fakir Mohan University, Balasore, India (Molecular Genetics & Genomics)
Professor J. V. J. Silva Júnior, Federal University of Santa Maria, Santa Maria-RS, Brazil (Virology, Immunology & Genetics)
Dr. Pradipta Saha, University of Burdwan, Burdwan, India (Microbiology)
Dr. S. Jayashree, KG College of Arts and Science, Coimbatore, India (Microbiology)
Dr. Om Prakash, National Centre For Cell Science, Pune, India (Microbiology)
Dr. Valasia Iakovoglou, University of Thessaly, Karditsa, Greece (Environmental Education & Forestry)
Dr. Nitin Kulkarni, ICFRE-Tropical Forest Research Institute, Jabalpur, India (Forest Entomology)
Professor José L. García Rodríguez, Polytechnic University of Madrid, Madrid, Spain (Hydraulics and Hydrology and Watershed)
Professor A. Vijaya Anand, Bharathiar University, Coimbatore, India (Phytos-Therapeutics)
Professor Ravindra Khaiwal, PGIMER, Chandigarh, India (Environmental & Occupational Health)
Professor P. S. Chaudhuri, Tripura University, Suryamaninagar, India (Earthworm Biology, Biodiversity & Ecology)
Dr. Afroz Alam, Banasthali Vidyapith, Vanasthali, India (Bryophytes & Environmental Botany)
Professor Avtar Singh Bimbraw, Punjab Agricultural University, Ludhiana, India (Agronomy)
Dr. A. K. Trivedi, ICAR - Central Institute for Subtropical Horticulture, Lucknow, India (Plant Physiology)
Dr. Surendra Pratap Singh, ICAR-Indian Institute of Sugarcane Research, Lucknow, India (Plant Physiology & Abiotic stresses)
Professor Renu Munjal, Chaudhary Charan Singh Haryana Agricultural University, Hisar, India (Plant Physiology & Genetics)
Dr. Mather A. Khan, University of Missouri,Columbia, USA (Molecular Plant Biology & Abiotech stress)
Dr. Rashid Ismael Hag Ibrahim, King Faisal University, Al-Ahsa, Saudi Arabia (Plant Molecular Biology and Genomics)
Dr. P. S. Harikumar, Centre for Water Resources Development and Management, Calicut, India (Environmental Monitoring)
Professor Abd El-Latif Hesham, Beni-Suef University, Beni-Suef, Egypt (Environmental Meta-Genome Biotechnology)

Journal of Environmental Biology, September 2024

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Journal of Environmental Biology
p-ISSN: 0254-8704 • e-ISSN: 2394-0379 • CODEN: JEBIDP JEB
Research & Development Division

The Research and Development (R&D) Division is a unique feature of the organization. A team of expert scientists in this division keeps
pace with the latest advancements made in different research fields, scrutinise reviewed and edited papers for unethical practices and
technical quality at each stage of publication to enhance the scientific merit of the research papers.

Consultant: Dr. R. B. Raizada, Scientist (Retired), Indian Institute of Toxicology Research, Lucknow - 226 001 (India).
Advisor: Dr. Amit Kumar Ghosh, Emeritus Scientist, Birbal Sahni Institute of Palaeosciences, Lucknow-226 007 (India).
Scientist-in-charge: Dr. Sumati Gaumat, Journal of Environmental Biology, Lucknow - 226 022 (India).
Assistant Scientist: Dr. Purnima Raizada, Journal of Environmental Biology, Lucknow - 226 022 (India).

Panel of Reviewers of 45 (5) September 2024

The following scientists acted as reviewers for the papers published in September issue of the Journal i.e., 45 (5) 2024
besides the Editorial Board Members. Our R&D division scientists further rechecked all the papers before publication.
To all of them, Journal of Environmental Biology thank for their valued services.

Professor Alagu Manickavelu, Central University of Kerala, Kasaragod, India

Professor Ghazwan Faisal Fadhil, University of Duhok, Duhok, Iraq
Professor Kalidas Upadhyaya, Mizoram University (A Central University), Aizawl, India
Professor L. N. Kakati, Assam Down Town University, Guwahati, india
Professor Sadanand Mallappa Yamakanamardi, University of Mysore, Mysore, India
Major Dr. N. Arun Nagendran, Thiagarajar College, Madurai, India
Dr. Ajay Kumar Maru, Anand Agricultural University, Anand, India
Dr. Amit Choudhary, Punjab Agricultural University, Ludhiana, India
Dr. Anchal Dass, ICAR-Indian Agricultural Research Institute (IARI), New Delhi, India
Dr. Andrew Flores, National Institute of Forestry, Agricultural and Livestock Research, Aldama, Mexico
Dr. Anilkumar Gopinathan, Vellore Institute of Technology, Vellore, India
Dr. Aniruddha Saha, University of North Bengal, Darjeeling, India
Dr. Anita Babbar, Jawaharlal Nehru Krishi Vishwa Vidyalaya, Jabalpur, India
Dr. Anju Kamra, ICAR-Indian Agricultural Research Institute, New Delhi, India
Dr. C. Valli Nachiyar, Meenakshi Academy of Higher Education and Research, Chennai, India
Dr. J. Helan Chandra, Jeppiaar Engineering College, Chennai, India
Dr. J. Praveenraj, ICAR-Central Island Agricultural Research Institute, Port Blair, India
Dr. Jaya Madhuri, Sri Padmavati Mahila Visvavidyalayam, Tirupati, India
Dr. Jaydeep Halder, ICAR-Indian Institute of Vegetable Research, Varanasi, India
Dr. Jyotirmaya Sahoo, Brahmanand P.G. College, Hamirpur, India

Contd......
Journal of Environmental Biology, September 2024
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Journal of Environmental Biology
p-ISSN: 0254-8704 • e-ISSN: 2394-0379 • CODEN: JEBIDP JEB
Dr. Mahender Singh, Sher-e-Kashmir University of Agricultural Sciences & Technology of Jammu, Jammu, India
Dr. Manjunatha Gowda Thondihalu, ICAR- Indian Institute of Vegetable Research, Varanasi, India
Dr. Moovendhan, Saveetha Institute of Medical and Technical Sciences (SIMATS), Chennai, India
Dr. Muthukumar. M., ICAR-Central Institute for Subtropical Horticulture, Lucknow, india
Dr. Naseema Rahman, RARS, AAU, Shillongani, Nagaon, India
Dr. Neelavannan. K., Indian Institute of Technology, Kanpur, India
Dr. P. K. Pradhan, ICAR- National Bureau of Fish Genetic Resources, Lucknow, India
Dr. Pankaj Kumar, ICAR-Research Complex for Eastern Region, Patna, India
Dr. Prem Kumar, ICAR-Central Institute of Fisheries Education, Mumbai, India
Dr. R. Valarmathi, ICAR-Sugarcane Breeding Institute, Coimbatore, India
Dr. Rajkumar, ICAR-Central Plantation Crops Research Institute, Kasaragod, India
Dr. Ramesh Kumar, ICAR-Indian Institute of Maize Research, Ludhiana, India
Dr. Rashmi Mahalle, Chungnam National University, Daejeon, South Korea
Dr. S. Satpathy, ICAR-Central Research Institute for Jute and Allied Fibres, Barrackpore, India
Dr. Samart K., M. S. Ramaiah Institute of Technology, Bangalore, India
Dr. Shravan M. Haldhar, ICAR-Central Institute for Arid Horticulture, Bikaner, India
Dr. Subhendu Jash, Bidhan Chandra Krishi Viswavidyalaya, Jhargram, India
Dr. T. Krishnakumar, ICAR-Central Tuber Crops Research Institute, Thiruvananthapuram, India
Dr. Teekam Singh, ICAR-Indian Agricultural Research Institute, New Delhi, India
Dr. Tulsi Saran Ghimiray, Uttar Banga Krishi Viswavidyalaya, Cooch Behar, India
Dr. Ujjwal Layek, Rampurhat College, Birbhum, India
Dr. Vikas Kumar, ICAR-Central Inland Fisheries Research Institute (ICAR-CIFRI), Barrackpore, India
Dr. Vikas Ramteke, Shaheed Gundadhoor College of Agriculture & Res. Station, Kumarawand, India
Dr. Zothansiama, Mizoram University, Aizawl, India

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Journal of Environmental Biology
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CONTENTS
Volume 45, Number 5, September 2024
WOS - Impact Factor : 0.6 Scopus Impact Factor : 0.703 WOS - JCI : 0.12 NAAS : 6.70 SJR : 0.23 H Index : 61

REVIEW ARTICLE
487-497 Cassava breeding: Classical to recent breeding approaches for food, industry and climate resilience
M. Velmurugan, R. Janaharshini, C. Indu Rani, S.R. Venkatachalam and P.A. Saravanan

ORIGINAL RESEARCH PAPERS

Occupational Toxicology/Public Health
498-506 Biological monitoring of exposure to benzene in water pipe smokers of rural Western Uttar Pradesh
(India)
Y. Verma, L.M. Vashistha, Mohd. Suaib and S.V.S. Rana

Medical Microbiology
507-514 Biofilm mediated antibiotic resistant oral bacteria among Parkinson's patients
J. Joel, P. Xavier, J.S. Pillai, T.S. Sujitha, A. Iyer, S. Sree and S. Murugan

Environmental Pollution
515-524 Microplastic pollution in the surface water of Yele Mallappa Shetty Lake, Bengaluru: first report
N.S. Kaviyarasi, V. Prasanna, S. Abitha and A.T. Anifowoshe

Animal Physiology
525-533 Ameliorative extract Syzygium cumini seed extract on lipid peroxidation and antioxidant activity
in alloxan induced diabetic Wistar albino rats
E. Kavitha and M. Sendhilvadivu

Shellfish Immunology
534-541 Short-term dietary supplementation of β-glucan and chitosan modulates the immune response
in freshwater prawn, Macrobrachium rosenbergii (De Man, 1879)
S. Sahoo, M.R. Badhe, A. Paul, P.K. Sahoo, K.C. Das, D. Panda, B.R. Pillai, S. Baliarsingh,
B.B. Patnaik and J. Mohanty

Fisheries and Aquaculture

542-550 Effect of stocking density and feeding regimes on physiological recovery in stunted Labeo rohita
fingerlings reared in cages
V.K. Paswan, K.D. Rawat, P.P. Srivastava, M.D. Aklakur, S.S. Lingam, S. Sangavi and M. Kumar

551-557 Influence of different stocking densities of pearlspot (Etroplus suratensis) on plankton diversity
indices of biofilm-based rearing system
S.R. Yadav, B.R. Chavan, N.K. Chadha, P.S. Bodake, K.K. Krishnani, P.B. Sawant and R. Bhosle

Journal of Environmental Biology, September 2024

 ®
Journal of Environmental Biology
p-ISSN: 0254-8704 • e-ISSN: 2394-0379 • CODEN: JEBIDP JEB
Ecology
558-564 Nest architecture of stingless bee, Tetragonula iridipennis Smith from Assam, North East India
P.S. Saranya, S. Borkataki, S. Sen, M.K. Deka, A. Devee, K. Das, B. Bhattacharyya,
R.R. Taye, M.D. Reddy and S.P. Nanda

565-575 Phyto-sociological changes in the Goima Forest, Gujarat due to human disturbances and
their implications for conservation
S.S. Malek, M.H. Patel, K.R. Rathod, S.K. Jha, B.S. Desai and M.B. Tandel

Ecosystem Valuation
576-585 Economic valuation of cultural ecosystem services: A case of tropical reservoir ecosystem
M. Meharoof, V.K. Yadav, A. Sharma, V. Anitha, T.T. Paul, L. Paul and C. P. Dave

Genetics and Plant Breeding

586-594 CoC 25–An early maturing high-yielding and red rot-resistant sugarcane variety suitable for
the East Coast Zone of India
S. Ganapathy, R. Latha, R.S. Purushothaman, V. Ravichandran, J. Jayakumar,
V. Karunakaran and C. Appunu

595-602 Accelerated development of maize inbred lines suitable for high density through doubled haploid
technology
H. Kaur, S. Sandhu, G. Singh, F. Khan, U.P. Praba and G. Kaur

Entomology
603-611 Effect of biotic and abiotic factors on the population dynamics of Nilaparvata lugens in the
middle Gangetic Plains of India
K.R. Sharma, S.V.S. Raju, S.K. Singh, R. Singh, U. Chandra, P.K. Dalal and R. Kumar

Namatology
612-618 Performance of tomato cultivars grafted on root-knot nematode resistant Solanum torvum
rootstock for growth and yield parameters
K. Sindhuja, S. Mallesh, P. Holajjer, G. Jyothi and S. Praneeth

619-625 Screening of newly isolated indigenous entomopathogenic nematodes against Spodoptera litura
Fabricius (Lepidoptera: Noctuidae)
R. Pervez, D. Sagar and Rajkumar

Agrometeorology
626-634 Evaluating influence of weather on Ascochyta blight severity in chickpea using correlation
network, regression and principal component analysis
B. Biswas, S. Kashyap, C. Kaur and R.S. Bal

Horticulture
635-644 Nutrient responsiveness and correlation analysis of cashew (Anacardium occidentale L.) cv.
Balabhadra for vegetative, reproductive traits and nut yield under coastal Odisha condition
C. Jena, P.K. Panda, K. Sethi, R.K. Nayak and R.K. Panda

Journal of Environmental Biology, September 2024

Journal of Environmental Biology ®
p-ISSN: 0254-8704 • e-ISSN: 2394-0379 • CODEN: JEBIDP
JEB
Original Research Paper J. Environ. Biol., 2024
Volume 45 Issue 5 September 2024 pp. 507-514 © Triveni Enterprises, Lucknow (India)
DOI: http://doi.org/10.22438/jeb/45/5/MRN-5483 Journal website : www.jeb.co.in « E-mail : editor@jeb.co.in

Biofilm mediated antibiotic resistant oral bacteria

among Parkinson's patients
J. Joel1, P. Xavier2, J.S. Pillai3, T.S. Sujitha1, A. Iyer1, S. Sree1 and S. Murugan1*
1
Department of Biotechnology, Karunya Institute of Technology and Sciences, Coimbatore -641 114, India
2
Department of Mathematics, Karunya Institute of Technology and Sciences, Coimbatore -641 114, India
3
Department of Medical Laboratory Science, Komar University of Science and Technology, Sulaimaniyah, Kurddistan, 46001, Iraq
Received: 16 April 2024 Revised: 26 May 2024 Accepted: 10 July 2024
*Corresponding Author Email: micromurugans@gmail.com *ORCiD: https://orcid.org/0000-0002-2432-1883

Abstract
Aim: The aim of this study was to examine the oral microbe biofilm and antibiotic resistance in individuals with Parkinson's disease compared to those
without the condition.

Methodology: In this study, the oral bacteria of older patients with Parkinson's disease and those without the condition were examined for antibiotic
resistance and biofilm formation. In this study, the microbiologists examined oral samples collected from 33 individual, out of which 18 sufferred from
Parkinson's disease while the remaining 15 individuals were normal. This case involved the use of the Matrix-Assisted Laser Desorption/Ionization-Time
of Flight (MALDI-TOF) technology to identify six different species.
Results: The analysis of oral samples showed the presence of six isolates viz. Staphylococcus epidermis, S. auricularis, S. simiae, Panebacillus
thiaminolyticus, P. aeruginosa and Bacillus cereus. Out of these, P. thiaminolyticus was absent in the control group. The incidence of oral microorganisms
was somewhat higher in Parkinson's disease patients than control individuals, however, there was no discernible variation in the oral bacterial strains
found in the two research groups. The isolates underwent further analysis following Congo Red Agar and Tissue Culture Plate methods and showed
positive result for biofilm formation. Each isolate found in the Parkinson's disease groups were found resistant to at least five antibiotics used.

Interpretation: The ability to produce biofilm was present in approximately 83.3% of the isolates from the Parkinson's disease group and 80% of those
from the control group. This study provides a deeper understanding of the relationship between biofilm-producing, antibiotic-resistant oral bacteria and
Parkinson's disease, and also address the need for effective management of oral hygiene in Parkinson’s patients.

Key words: Antibiotic resistance, Biofilm, Oral microbiota, Oral health, Parkinson’s disease

Development of
antibacterial Collection of oral samples
strategies from individuals Identification of six bacterial
in combating species from oral sample via
drug-resistant MALDI-TOF technology
bacteria for the
effective Staphylococcus epidermis, S. auricularis,
management of Testing of antibiotic S. simiae, Pseudomonas aeruginosa,
oral hygeine in resistance of isolates Bacillus cereus and
Parkinson's Panebacillus thiaminolyticus
patients
Comparison of bacterial species
between Parkinson disease and
Examination of isolates
Non-Parkinson disease groups
for biofilm development
How to cite: Joel, J., P. Xavier, J.S. Pillai, T.S. Sujitha, A. Iyer, S. Sree and S. Murugan: Biofilm mediated antibiotic resistant oral bacteria among Parkinson's patients. J.
Environ. Biol., 45, 507-514 (2024).
(Educational Services Set-up)
 J. Joel et al.: Antibiotic resistant oral bacteria in Parkinson’s patients

Introduction stands out as a prominent cause of mortality in Parkinson's disease,

with an elevated risk attributed to oral dysbiosis resulting from
Parkinson disease is a age-related motor illnesses, inadequate oral hygiene (Rozas et al., 2021). In view of the above,
prevalent with advancing age in people (Van Den Eeden et al., the aim of this study was to examine and compare the oral microbe
2003). People suffering from Parkinson disease show varied biofilm and antibiotic resistance in Parkinson's disease patients with
symptoms, both motor and non-motor with Tremor, Bradykinesia, normal indviduals.
and stiffness being the most common motor symptoms (Jiménez
and Vinger, 2012), which may obstruct automated minor hand Materials and Methods
motions (Schwarz et al., 2006), including the capacity to brush
teeth leading to oral health deterioration (Müller et al., 2011). Study subjects and sampling: Each participant in this research
These symptoms have been linked to enteric nervous system received questionnaire comprising information about their
neuropathology, which is associated with the brain protein alpha- demographics, age, gender, symptoms, duration of disease and
synuclein. Identical changes have been observed in the upper dental hygiene. In total thirty-three (No=33) saliva samples from
oesophagus, larynx and oropharynx mucosal sensory nerve the oral cavity were collected, 15 from Parkinson's disease
terminals. Parkinson's disease often manifests after the age of 40 patients (three were removed), and 15 from normal participants.
and primarily affects males (Mu et al., 2017). Because of extrinsic Since the sampling was non-invasive, all human volunteers and
variables like germs in the upper respiratory tract and dental professionals gave written consent before sample
gastrointestinal tract, olfactory and gastrointestinal tissues may collection. The individuals in the Parkinson's disease group met the
get damaged due to sickness (Fansano et al., 2015). This may standard diagnostic criteria for late-onset Parkinson's disease,
initiate rapid degeneration of nerve cells, leading to Parkinson's which include bradykinesia, stiffness, or a resting tremor, and had
disease (Lema Tomé et al., 2013). Several studies have been previously been diagnosed by a neurologist (Schwarz et al., 2006;
undertaken that effectively link the gut microbiota's function in Postuma et al., 2015). Participants with periodontal disease were
Parkinson's disease (Scheperjans et al., 2015; Nielsen et al., not excluded from the study, nor were those with any known
2021). conditions affecting the mouth, salivary glands, nose, throat or
ears. Additionally, individuals who had taken antibiotics within a
Periodontal disease, which has been connected to month prior to the sample collection date were also included.
Parkinson's disease (Müller et al., 2011; Kamer et al., 2020) has a There was no thorough clinical assessment of the subjects' oral
significant influence on the latter. Numerous studies have also cavity or dental health. Saliva samples were obtained by gently
suggested that oral microbiota may have a role in several human stroking the buccal and sublingual mucosa both sides of the mouth
illnesses, including diabetes and cardiovascular diseases using a sterile cotton swabs. Samples from this region were taken
(Kumar, 2017; Giordano et al., 2022). Patients with Parkinson's into consideration because of their close proximity to the parotid and
disease who have a disturbed oropharyngeal status may also see submandibular ducts. Cotton swabs containing samples were
repeatable changes in the salivary microbiota that set them apart sealed in sterile vials and delivered straight to the laboratory under
from normal. Chewing/ biting issues, loss of taste, tooth ice-cold conditions within 48 hr of sample collection (Byrne et al.,
movement, and xerostomia are all significant symptoms of 2022).
Parkinson's disease (Van Stiphout et al., 2018). Oral cavity issues
are one of the expanding non-motor signs and symptoms of Identification of bacteria using MALDI-TOF Mass Spectroscopy:
Parkinsonism (Simonet et al., 2022). Due to dental and MALDI-TOF technique was used to examine each isolate at the
periodontal conditions, it might be challenging for Parkinson's Microbiological Laboratory Pvt. Ltd., Coimbatore, India. The
disease patients to maintain good oral hygiene. There are several samples were inoculated at 37°C onto nutrient agar for 24 hr. A
reasons why patients suffering from Parkinson's disease cannot microtiter plate was used to hold each culture. A lysis solution was
maintain their dental hygiene. These include, motor impairment then added to the bacterial sediment, therefore one litre of. aliquot
(reduced dexterity of the arms and fingers may make it difficult to of the matrix solution—containing 2.5% trifluoroacetic acid and
do the necessary daily oral hygiene treatment), apathy, 50% acetonitrile diluted with alpha-ciano-4-hydroxy-cinamic acid
depression and dementia (Hanaoka and Kashihara, 2009; from Sigma-Aldrich®—was added. Nitrogen laser (337 nm) was
Vanbellingen et al., 2010; Debowes et al., 2013). used in the mass spectrometer to create a spectra for each
sample, following a straight path. The standard configuration for
Previous studies have reported deteriorated periodontal bacterial identification was employed to assess the spectra in the
health, more missing teeth, caries, and dental biofilm in patients mass range of 2000 to 20,000 m sec-1 using the MALDI Biotyper
suffering from Parkinson's disease as compared to healthy 2.0 application. Later the sample spectra were contrasted with the
individuals (Petersen, 2003; Einarsdóttir et al., 2009; Muller et al., database references.
2011). The microbes that form biofilms for defense are more
resistant to various classes of drugs (Rather et al., 2021). The Screening for microorganism producing biofilm
advantage of bacterial biofilms to an organism's survival processes
can be related to virulence, pathogenicity or antibiotic resistance Congo Red Agar method: Oral isolates were streaked on Brain
(Brandwein et al., 2016; Vestby et al., 2020). Aspiration pneumonia Heart Infusion agar, which consisted of 5% sucrose and 0.08%

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 J. Joel et al.: Antibiotic resistant oral bacteria in Parkinson’s patients

Congo Red dye. The plates were incubated for 24 hr at 37 °C are more likely to suffer from Parkinson’s disease than women.
(Bose et al., 2009). The isolates producing biofilms showed black Additionally, it was reported that each patient suffering from
colonies whereas the non-biofilm producing isolates developed Parkinson's disease experienced resting tremors.
red colonies.
The proportion of Parkinson's disease cases presenting
Tissue culture plate method: An overnight culture in nutrient various symptoms within the study group was analyzed, revealing
broth and a 1:100 dilution in BHI broth were used for the biofilm tremor as the most prevalent symptom, affecting all individuals
development experiment in microtiter wells. Using a flat-bottom (100%). Additionally, difficulty in walking (66.67%) and excessive
96-well polystyrene microtiter plate, a 200µl of cell suspension salivation (38.89%) were also commonly reported, while memory
was added to each well. Following a 48 hrs incubation period at loss (27.78%) and depression (11.11%) were less frequently
35˚C, the detached cells underwent three gentle rinses with observed among the affected individuals. Salivary microbes from
sterile distilled water. Subsequently, the bacteria adhered to the Parkinson’s disease patients and healthy individuals were
surface were stained using crystal violet, recleaned and de- compared (Table 1) showing S. epidermidis to be present in
stained with ethanol-acetone (95:5, v/v). Optical density was read 16.67% of PD individuals compared to 13.34% in the control
at 570 nm wavelength (OD) 570nm using 200µl of the combined group. S. auricularis was found in 5.56% of Parkinson's patients,
solution that was transferred to a 96-well microtiter plate (Pierce significantly lower than the 20.0% observed in the control group.
et al., 2008). Micro-ELISA Auto-reader recorded the absorbance. Notably, P. thiaminolyticus was detected in 33.33% of individuals
Each test was run thrice, and the mean OD570 value of the wells with Parkinson's disease but was absent in the control group.
that were tested was used. Based on the ODs in the BHI broth, the
biofilm formation was separated into three categories: biofilm B. cereus was present in 11.11% of Parkinson's patients,
non-formers (OD570<0.2), biofilm formers of weak level (OD570 whereas it was more prevalent in the control group (33.34%).
in the range of 0.2-1.0), and biofilm formers of strong level Finally, P. aeruginosa was present in 22.22% of Parkinson's
(OD570 >1.0) (Bose et al., 2009). patients and 26.67% of controls. These variations suggest that
Parkinson's disease may influence the composition of the oral
Antibiotic sensitivity test: The bacteria screened for biofilm microbiota, potentially impacting oral health and the propensity
production were further analysed for antibiotic susceptibility test. for certain infections. Saliva samples from both group showed the
A sterile cotton swab was dipped into the overnight culture, presence of Staphylococcus species viz., S. epidermidis, S.
employing the subsequent drugs: Imipenem (10 mcg), Linezolid auricularis, and S. simiae, The prevalence of microorganisms
(30 mcg), Methicillin (5 mcg), Minocycline (30 mcg), Ampicillin (10 across the two groups did not differ significantly, with the
mcg), Piperacillin-Tazobactam (100/10 mcg), Tigecycline (15 exception of P. thiaminolyticus, which was absent in control
mcg), Cefepime (30 mcg), Cefotaxime (30 mcg), Ceftazidime (30 participants. P. thiaminolyticus predominated (33.33%) in the
mcg), Co- Trimoxazole (25 mcg) and Ceftriaxone (30mcg) (Hi- saliva of Parkinson’s disease patients, but B. cereus was found in
Media, Mumbai). The Mueller-Hinton agar medium (Hi-Media, higher percentage (33.34%) of all other isolates in the saliva of
Mumbai) was thoroughly streaked with swabs, and the antibiotic normal patients. The presence of P. aeruginosa was similar in
disc was gently placed above it with the help of tweezers. The both patients. The identified oral bacterial species were tested for
plates were incubated at 37 °C for 24 hr. The inhibition zones on the existence of biofilms by Congo red agar plate method. The
the plates were checked after the incubation period. The zones oral isolates showed dry, black colonies that suggested the
were measured and interpreted in accordance with the Clinical formation of biofilms, while red colonies revealed the presence of
and Laboratory Standard Institute's Guidelines (Javiya et al., non-biofilm producers (Table 2).
2008; CLSI, 2016).
From the tissue culture plate analysis, a high prevalence
Statistical analysis: All experiments were performed in triplicate of biofilm was observed among oral isolates obtained from
and the data were analyzed using a Student's t-test. Statistical individuals with Parkinson's disease, with 61.29% of samples
significance was determined at a p-value threshold of 0.05.

Results and Discussion Table 1: Microbiota profiles in the oral cavity of individuals with and
without Parkinson’s disease
In total thirty-three (N=33) participants including 15
Microorganisms Parkinson’s Control (%)
Parkinson’s disease patients and 15 normal individuals (and 3
disease (%)
excluded) participated in this study. Participants suffering from
Parkinson’s disease were 50 years old. The prevalence of S. epidermidis 3 (16.67) 2 (13.34)
Parkinson's disease increases with advancing age, with a notable S. auricularis 1 (5.56) 3 (20.0)
rise observed in individuals aged 60 to 64 (33.33%) and those S. simiae 2 (11.11) 1 (6.67)
aged 65 and above (50%), according to the distribution among P. thiaminolyticus 6 (33.33) 0
Parkinson’s disease patients in the specified age groups. It has B. cereus 2 (11.11) 5 (33.34)
been found that illness incidence advances with age and that men P. aeruginosa 4 (22.22) 4 (26.67)

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 J. Joel et al.: Antibiotic resistant oral bacteria in Parkinson’s patients

Table 2: Prevalence of biofilm development among oral microflora in Parkinson’s disease and control populations
Parkinson’s disease Control
Microorganisms Biofilm Non-biofilm Biofilm Non-biofilm
Producing (%) Producing (%) Producing (%) Producing (%)
S. epidermidis 2 (66.67) 1 (33.33) 1 (50) 1 (50)
S. auricularis 1 (100) 0 2 (66.7) 1 (33.33)
S. simiae 1 (50) 1 (50) 1 (100) 0
P. thiaminolyticus 0 6 (100) - -
B. cereus 2 (100) 0 3 (60) 2 (40)
P. aeruginosa 3 (75) 1 (25) 4 (100) 0

Table 3: Biofilm-producing microorganism identification in Parkinson’s than women. Moisan et al. (2016) found that the male-to-female
disease and Non-Parkinson’s disease Individuals ratio for the disease increases with age, which is in line with the
results of the current investigation. Rozas et al. (2021),
Microorganisms Parkinson’s disease Non-Parkinson’s disease investigated the factors influencing the oral microbiota in
S. epidermidis + + individuals with Parkinson's disease. The findings revealed an
S. auricularis ++ ++ increased presence of opportunistic oral pathogens among the
S. simiae ++ + patients. The study identified specific factors, such as dysphagia
P. thiaminolyticus - -
and drooling (both with a significance level of p < 0.05), along with
salivary pH (p < 0.005), that had a significant impact on the beta-
B. cereus ++ +
diversity of soft tissues and composition of oral microbiota.
P. aeruginosa ++ ++
Previous research has demonstrated that non-oral species
Note: (+++) Strong, (++) Moderate, (+) Weak, (-) No biofilm production detected in the oral microbiota may function as a repository for
medically significant pathogens, rather than merely being the
result of contamination during sample collection (Botero et al.,
showing biofilm production. The optical density (OD) 2012; Souto and Colombo, 2008; Fritschi et al., 2008; Gonçalves
measurements of stained adherent bacteria was analyzed with a et al., 2009; Wang et al., 2023). However, it was observed that all
micro-ELISA auto reader operating at 570 nm. Based on OD the six isolates were sensitive to Imipenem and Piperacillin-
values, isolates were categorized as strong, moderate, weak, or tazobactam antibiotics.
non-biofilm producers. Staphylococcus species (S. epidermidis,
S. auricularis and S. simiae) and B. cereus showed varying Staphylococcus species such as S. auricularis, S.
degrees of biofilm production in both groups, with generally epidermidis and S. simiae have been found to inhabit the oral
higher levels observed in Parkinson's disease patients compared cavity, and under certain conditions, it can lead to localized or
to controls as shown in table 3. Notably, P. aeruginosa systemic infections (Kloos and Bannerman, 1994). For instance,
demonstrated significant biofilm production in both groups. S. auricularis, typically found in the ear, can cause infections if it
Notably, all oral isolates exhibited resistance to a minimum of five accesses sterile body sites; S. epidermidis, a common skin
antibiotics, as shown in Table 4. Table 5 presents the relationship commensal, can form biofilms on medical devices and contribute
between antibiotic resistance patterns and biofilm-forming oral to infections, particularly in immunocompromised individuals; and
microorganisms. Each microorganism displayed resistance to S. simiae, although less commonly discussed, can cause
multiple antibiotics, with B. cereus resistant to 7 antibiotics and P. infections if it enters the bloodstream or other sterile areas. The
aeruginosa resistant to 6 antibiotics, respectively (table 4). frequency of Staphylococcus species in oral samples, as
Staphylococcus species, including S. auricularis, S. epidermidis, reported by Simes-Silva et al. (2018) and Smith et al. (2011),
and S. simiae, exhibited resistance to five antibiotics each. This supports their common presence in the oral cavity. Their
suggests a concerning trend of multidrug resistance among persistence can be attributed to mechanisms such as biofilm
biofilm-forming oral microorganisms associated with Parkinson's formation, which protects them from host immune responses and
disease, emphasizing the need for effective antimicrobial antibiotics (Beatriz et al., 1999; Bose et al., 2009); adhesion to
strategies in managing oral health in patients. epithelial cells facilitated by surface proteins; and the
development of antibiotic resistance, particularly in species like S.
Approximately, 0.02% people above 65 years of age all epidermidis.
over the world suffer from Parkinson's disease caused by
substantia nigra of the brain where nerve cells slowly die off. Coagulase Negative Staphylococci (CoNS), especially S.
About 88.8% of the Parkinson’s disease patients in this research epidermidis, pose a significant threat due to their ability to develop
were males, while the remaining 11.2% were females. According antibiotic resistance and form biofilms. These bacteria can
to Moisan et al. (2016) and Roohani et al. (2013), men are more adhere to oral surfaces, contributing to periodontal disease and
likely to suffer from Parkinson's disease almost 1.6 times more complicating treatment due to their resistance to common
510 Journal of Environmental Biology, September 2024
 J. Joel et al.: Antibiotic resistant oral bacteria in Parkinson’s patients
Table 4: Antimicrobial pattern for oral microorganisms isolated from Parkinson’s disease subjects
Antibiotics S. epidermidis S. auricularis S. simiae P. thiaminolyticus P. aeruginosa B. cereus
AMP R R R R R R
CAZ R R R R S R
MET R R R R R R
CTX R R R I I R
CPM R R R R S R
CTR I R R R S R
TGC S S S S R S
COT I I I I R R
LZ S S R S R S
MI S I I S R I
PIT S S S S S S
IPM S S S S S S
*AMP- Ampicillin; CAZ- Ceftazidime; MET- Methicillin; CTX- Cefotaxime; CPM- Cefepime; CTR- Ceftriaxone; COT- Co-Trimoxazole; TGC-
Tigecycline; LZ- Linezolid; MI- Minocycline; IMP- Imipenem; PIT- Piperacillin-tazobactam. **R- resistant; I- Intermediate; S- Sensitive

antibiotics like β-lactams, gentamicin and erythromycin (Asante Table 5: Relationship between the pattern of antibiotic resistance and the
et al., 2020). These mechanisms highlight the adaptability of biofilm-forming oral microorganisms
Staphylococci to the oral environment and their potential role in Microorganisms Parkinson’s disease
oral and systemic infections, underscoring the importance of
monitoring and understanding their behavior to manage and B. cereus AMP, CAZ, MET, CTX, CPM, CTR, COT (7)
P. aeruginosa AMP, MET, TGC, COT, LZ, MI (6)
prevent infections effectively. Therefore, due to the presence of
S. auricularis AMP, CAZ, MET, CTX, CPM, CTR (6)
CoNS in the oral cavity, Parkinson's patients may develop S. epidermidis AMP, CAZ, MET, CTX, CPM (5)
periodontal diseases (Manandhar et al., 2021). S. auricularis has S. simiae AMP, CAZ, MET, CTX, CPM (5)
hardly ever been found in oral infectious diseases (Braga et al.,
2005). Ouyang et al. (2024) reported the presence of P. *AMP- Ampicillin; CAZ- Ceftazidime; MET- Methicillin; CTX- Cefotaxime;
thiaminolyticus in an 80-year-old Parkinson's disease patient, CPM- Cefepime; CTR- Ceftriaxone; COT- Co-Trimoxazole; TGC-
Tigecycline; LZ- Linezolid; MI- Minocycline
which is in line with the present findings. This peculiar spore-
forming bacteria, like Paenibacillus sp. strain VT-400, which was
identified in the saliva of patients with acute lymphoblastic saliva includes proteins or glycoproteins that aid in the formation
leukaemia, has not been reported in humans (Tetz et al., 2015). P. of enamel layer, bacteria to cling to surfaces to form plaque (Holt
thiaminolyticus in oral samples of Parkinson's patients may be the et al., 1988; Zimmerman et al., 2013; Fiorillo, 2019; Hanisch et al.,
first of its kind. Furthermore, before Paenibacillus species were 2019). Microbes producing biofilms have caused numerous
identified as human pathogens, they were known to cause problems in agriculture, medicine and daily living (Shineman et
respiratory and urinary tract infections (Kim et al., 2010; Padhi et al., 2014). Germs that form biofilms are also assumed to be
al., 2013). resistant to antibiotics due in part to their slower rate of cell
proliferation when compared to free-living planktonic cells
Patients with periodontitis reported a notably higher (Chuard et al., 1993). P. aeruginosa and S. epidermidis were
prevalence of P. aeruginosa in their saliva and subgingival biofilm shown to be poor biofilm producers in the oral bacteria of
samples, according to Souto et al. (2014). The bacterium was Parkinson's patients, but B. cereus, S. auricularis, and S. simiae
found in both the participants in this study, indicating their role in were shown to be moderate biofilm builders (Hsueh et al., 2006;
the etiopathogenesis of periodontal diseases in Parkinson's Okajima et al., 2006). P. thiaminolyticus isolated from Parkinson’s
patients. Bakke et al. (2011) found that dental plaque, food disease was unique as it did not form biofilm. Santos et al. (2015)
particles, and periodontal health are more evident in patients with revealed the prevalence of Staphylococcus spp. in the
advanced Parkinson's disease (Hansen et al. 1993). Food debris subgingival biofilm. B. cereus in this study showed resistance to
may be the cause of B. cereus colonization in the oral cavity, most of the antibiotics tested, similar to report of Owusu-
which may be overlooked at early stages of pulmonary and Kwarteng et al. (2017). S. auricularis and P. aeruginosa both
systemic infections in immunocompromised individuals' showed resistance to Ampicillin, Methicillin, Tigecycline, Co-
development (El Saleeby et al., 2004). The salivary flow rate is Trimoxazole, Linezolid and Minocycline (Brown et al., 2012). The
essential for maintaining optimal oral health in Parkinson's presence of spores has significantly contributed to both the
patients because it plays a preventative function against plaque persistence of infections and the spread of antibiotic resistance.
and germs from mucosal and dental surfaces (Kennedy et al., Five different antibiotics were resistant to P. thiaminolyticus
1994; Müller et al., 2011). Previous studies have reported that (Barra-Carrasco et al., 2014). Furthermore, it was found that

511 Journal of Environmental Biology, September 2024

 J. Joel et al.: Antibiotic resistant oral bacteria in Parkinson’s patients

among the Staphylococcus species isolated from oral samples, Authors’ contribution: J. Joel: Contributed to the research idea
S. auricularis was resistant to Ampicillin, Ceftazidime, Methicillin, and writing of the manuscript; P. Xavier: Contributed to the
Cefotaxime, Cefepime and Ceftriaxone, while S. epidermidis and research idea including framing of questionnaire for collecting
S. simiae were both resistant to Ampicillin, Ceftazidime, primary data; J.S. Pillai: Contributed to the research article
Methicillin, Cefotaxime and Cefepime. Conversely, all species of through writing; T.S. Sujitha: Contributed by writing the research
Staphylococcus were found to be susceptible to linezolid, article and conducting the research work; S. Sree: Collaborated
aligning with the findings of Abdel Halim et al. (2018). This in writing and editing the manuscript; A. Iyer: Assisted in writing
consistency underscores linezolid's effectiveness as a treatment and editing the manuscript; S. Murugan: Provided the initial
option against Staphylococcus infections, highlighting its research idea, assisted in coordination, and participated in the
potential as a reliable antibiotic in the face of rising antibiotic final correction of the paper.
resistance.
Funding: Not applicable.
The susceptibility of Staphylococcus species to linezolid
reinforces its role in clinical settings, particularly for infections that Research content: The research content of manuscript is
are resistant to other antibiotics. Most people agree that clinical original and has not been published elsewhere.
isolates with higher antibiotic resistance levels arise from repeated
medication exposure (Antoniadou et al., 2013). Cantas et al. (2013) Ethical approval: The researchers had maintained anonymity
suggest that there might be a connection between the environment with verbal consent from the patients under the meticulous
and the development of antibiotic resistance in microorganisms. In guidance of a medical expert, who also requested anonymity.
a similar study, Fleury et al. (2021), observed higher abundance of Since oral samples were collected through non-invasive
certain bacterial species, including Streptococcus mutans, procedures, no formal ethical approval was required. However,
Kingellaoralis, Actinomyces AFQC_s, Veillonella AFUJ_s, the study adhered to ethical standards, ensuring the utmost
Scardovia, Lactobacillaceae, Negativicutes, and Firmicutes were respect for the rights and privacy of the participants. The research
observed in patients. team remained committed to upholding ethical principles and
safeguarding the integrity of the study while contributing valuable
Conversely, there was a lower abundance of Treponema insights to the understanding of Parkinson's disease.
KE332528_s, Lachnospiraceae AM420052_s, and the phylum
SR1 in the same patient group (Fleury et al. 2021).The Conflict of interest: The authors declare that there is no conflict
heightened prevalence of multidrug-resistant CoNS among of interest.
Parkinson patients, as indicated by our research, is concerning.
Furthermore, this observation suggests a correlation with Data availability: Not applicable.
compromised dental hygiene and deteriorating oral health, likely
attributable to deficiencies stemming from Parkinson's disease, Consent to publish: All authors agree to publish the paper in
such as impaired motor control affecting oral care practices. Journal of Environmental Biology.

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