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Formaldehyde exposure and atmospheric biomonitoring with lichen Cladonia verticillaris in an anatomy laboratory

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Abstract

Formaldehyde is one of the most toxic contaminants of indoor environments and very common in the anatomy laboratory. In this work, we investigated the level of formaldehyde exposure to staff and students who attended an anatomy lab and in nearby environments in the same university building. We also performed atmospheric biomonitoring of the sites with the lichen Cladonia verticillaris. Quantification samplings were performed over four weeks, on 7 days with and 7 days without practical classes, totaling 70 samples. The samples were collected in five different locations, three points inside the laboratory and two points outside the laboratory, representing nearby and susceptible environments to contamination. The results showed CHOH concentrations from 0.20–3.76 ppmv for days with practical courses and 0.17–3.06 ppmv for days without practical classes. Although the laboratory was more contaminated than the surrounding environments, the concentration of formaldehyde in these areas is not negligible, showing a dispersion of formaldehyde from the laboratory. Potential dose (PD) and cancer risk (CR) were calculated for an individual exposed to the same levels analyzed for 8 h daily and 30 years of work. The study on C. verticillaris lasted 90 days and evaluated the variation of chlorophyll and pheophytin (photosynthetic pigments). The results showed a significant difference in the production of chlorophylls a and b and total chlorophyll when compared to control, and there was also a progressive increase of the total pheophytin/total chlorophyll ratio. The results also showed the correlation between the increase in chlorophylls and the studied environments with less ventilation since these places provided greater accumulation of formaldehyde in the long run. Thus, measurable evidence was obtained of biological disorders in a living organism caused by exposure to formaldehyde.

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References

  • ACGIH – American Conference of Governmental and Industrial Hygienists (2001) Guidelines for classification of occupational carcinogenicity, 7th edn Cincinnati

    Google Scholar 

  • ACGIH – American Conference of Governmental and Industrial Hygienists (2006) Limites de exposição ocupacional (TLVs) para substâncias químicas e agentes físicos & índices biológicos de exposição. Translation. ABHO, São Paulo

    Google Scholar 

  • Ahmed HO (2011) Preliminary study: Formaldehyde exposure in laboratories of Sharjah University in UAE. Indian J Occup Environ Med 15:33–37

    Article  Google Scholar 

  • Ahti TS, Xavier-Filho L (1993) The lichen family Cladoniaceae in Paraiba, Pernambuco and Sergipe, northeast Brazil. Bryophyte Divers Evol 7:55–70. https://doi.org/10.11646/bde.7.1.6

    Article  Google Scholar 

  • Al-Alam J, Chbani A, Faljoun Z, Millet M (2019) The use of vegetation, bees, and snails as important tools for the biomonitoring of atmospheric pollution—a review. Environ Sci Pollut Res 26:9391–9408. https://doi.org/10.1007/s11356-019-04388-8

    Article  CAS  Google Scholar 

  • Barták M, Vráblīková-cemprīková H, Štepigovà J, Hájek J, Váczi P, Večeřová K (2008) Duration of irradiation rather than quantity and frequency of high irradiance inhibits photosynthetic processes in the lichen Lasallia pustulata. Photosynthetica. 46. https://doi.org/10.1007/s11099-008-0027-7

  • Bernstein JA, Alexis NB, Hyacinth B, Fritz P, Horner EL, Ning M, Mason S, Nel A, Oullette J, Reijula K, Reponen T, Seltzer J, Smith A (2008) The health effects of nonindustrial indoor air pollution. J Allergy Clin Immunol 121:585–591. https://doi.org/10.1016/j.jaci.2007.10.045

    Article  CAS  Google Scholar 

  • Bettini DR (2006) Qualidade do ar em laboratório climatizado de anatomia patológica: avaliação de agentes químicos. Dissertation. Universidade Estadual do Rio de janeiro

  • Brasil (1978) Norma Brasileira NR15–Segurança e Medicina do Trabalho–Atividades e Operações Insalubres. www.mte.gov.br/legislacao/normas_regulamentadoras/nr_15.pdf. Accessed Apr 2020

  • Carreras HA, Gudino GL, Pignata ML (1998) Comparative biomonitoring of atmospheric quality in zones of Cordoba city (Argentina) employing the transplanted lichen Usnea sp. Environ Pollut 103:317–325. https://doi.org/10.1016/S0269-7491(98)00116-X

    Article  CAS  Google Scholar 

  • Cruz MB, Pereira EC, Silva NH, Mota-Filho FO, Martins MCB (2009) Monitoramento da ação do formaldeído sobre Cladia aggregata (líquen) em condições de laboratório. Caminhos de Geografia 10:76–87

    Google Scholar 

  • Cruz LP, Luz SR, Campos VP, Santana FO, Alves RS (2020) Determination and risk assessment of formaldehyde and acetaldehyde in the ambient air of gas stations in Salvador, Bahia, Brazil. J Braz Chem Soc. https://doi.org/10.21577/0103-5053.20190278

  • Dehghani M, Khodabakhshi A, Taghizadeh MM, Hashemi H, Rastgoo E (2015) Modelling of formaldehyde dispersion in the industrial park air using GIS. Int J Environ Waste Manag 16:293. https://doi.org/10.1504/IJEWM.2015.074933

    Article  CAS  Google Scholar 

  • Durongphan A, Amornmettajit N, Rungruang J, Nitimanee J, Panichareon B (2020) One academic year laboratory and student breathing zone formaldehyde level, measured by gas-piston hand pump at gross anatomy laboratory, Siriraj Hospital, Thailand. Environ Sci Pollut Res 27:16521–16527. https://doi.org/10.1007/s11356-020-08199-0

    Article  CAS  Google Scholar 

  • Eslami F, Salari M, Dehghani MH, Dargahi A, Nazmara S, Beheshti A (2019) Relationship of formaldehyde concentration in ambient air with CO, NO2, O3, temperature and humidity: modeling by response surface model. Arch Hyg Sci 8:9–16

    Article  CAS  Google Scholar 

  • Franklin SDL, Bettini DR, Mattos UADO, Fortes JDN (2009) Avaliação das condições ambientais no laboratório de anatomia patológica de um hospital universitário no município do Rio de Janeiro. J Bras Patol Med Lab 45:463–470. https://doi.org/10.1590/S1676-24442009000600005

    Article  Google Scholar 

  • Gonzalez CM, Orellana LC, Casanovas SS, Pignata L (1998) Environmental conditions and chemical response of a transplanted lichen to an urban area. J Environ Manag 53:73–81. https://doi.org/10.1006/jema.1998.0194

    Article  Google Scholar 

  • Gunson TH, Smith HR, Vinciullo C (2011) Assessment and management of chemical exposure in the Mohs laboratory. Dermatol Surg 37:1–9. https://doi.org/10.1111/j.1524-4725.2010.01807.x

    Article  CAS  Google Scholar 

  • Gurgatz B, Moreira AB, Antonia C, Reis R (2017) Teloschistes flavicans (sw.) Norman como indicador de poluição atmosférica em Paranaguá – PR. Rev Bras Ciênc Ambient (Online). https://doi.org/10.5327/Z2176-947820170105

  • Hammer N, Löffler S, Feja C, Sandrock M, Schmidt W, Bechmann I, Steinke H (2012) Ethanol-glycerin fixation with thymol conservation: a potential alternative to formaldehyde and phenol embalming. Anat Sci Educ 5:225–233. https://doi.org/10.1002/ase.1270

    Article  Google Scholar 

  • Hampp R, Cardoso N, Fleig M, Grüninger W (2018) Vitality of lichens under different light climates in an Araucaria forest (Pró-Mata RS, South Brazil) as determined by chlorophyll fluorescence. Acta Bot Bras 32:188–197. https://doi.org/10.1590/0102-33062017abb0187

    Article  Google Scholar 

  • Homwutthiwong K, Ongwandee M (2017) Investigation of formaldehyde in gross anatomy laboratory: area-based and exposure levels, ventilation, health risk and clinical symptoms. App Envi Res. https://doi.org/10.35762/AER.2017.39.3.8

  • IARC - International Agency for Research on Cancer (2012) Monographs on the evaluation of carcinogenic risks to humans, Volumes 100F. Chem Agents Relat Occup 249:294

    Google Scholar 

  • IBGE (Instituto Brasileiro de Geografia e Estatística (2015) Tabelas de mortalidade completa, 2015. https://biblioteca.ibge.gov.br/visualizacao/periodicos/3097/tcmb_2015.pdf. Acessed Aug 2018

  • INCA- Instituto Nacional do Câncer (2013) Diretrizes para a vigilância do câncer relacionado ao trabalho. Ministério da Saúde, Rio de Janeiro

    Google Scholar 

  • Kalanjati VP, Prasetiowati L, Alimsardjono H (2012) The use of lower formalin-containing embalming solution for anatomy cadaver preparation. Med J Indonesia. https://doi.org/10.13181/mji.v21i4.505

  • Klein RC, King C, Castagna P (2014) Controlling formaldehyde exposures in an academic gross anatomy laboratory. J Occup Environ Hyg 11:127–132. https://doi.org/10.1080/15459624.2013.816432

    Article  CAS  Google Scholar 

  • Legaz ME, Vicente C, Ascaso C, Pereira EC, Xavier Filho L (1986) Pigment analysis of sun and shade populations of Cladonia verticillaris. Biochem Syst Ecol 14:575–580. https://doi.org/10.1023/A:1005673715916

    Article  Google Scholar 

  • Levin AG, Pignata ML (1995) Ramalina ecklonii as bioindicator of atmospheric pollution in Argentina. Can J Bot 73:1196–1202. https://doi.org/10.1139/b95-129

    Article  Google Scholar 

  • Mota-filho FO, Pereira EC, Lima ES, Silva NHF (2007) Influência de poluentes atmosféricos em Belo Jardim (PE) utilizando Cladonia verticillaris (líquen) como biomonitor. Quím Nova 30:1072–1076. https://doi.org/10.1590/S0100-40422007000500004

    Article  CAS  Google Scholar 

  • Nash TH (2008) Lichen Biology. Cambridge University, Cambridge

    Book  Google Scholar 

  • NIOSH - National Institute for Occupational Safety and Health (1982) Health hazard evaluation. National Institute for Occupational Safety and Health, Cincinnati (Report no. HETA 82-045-1108)

    Google Scholar 

  • Ochs SDM, Grotz LDO, Factorine LS, Rodrigues MR, Netto ADP (2012) Occupational exposure to formaldehyde in an institute of morphology in Brazil: a comparison of area and personal sampling. Environ Sci Pollut Res 19:2813–2819. https://doi.org/10.1007/s11356-012-0786-3

    Article  CAS  Google Scholar 

  • OSHA – Occupational Safety and Health Administration (2013) Substance technical guidelines for formalin. Toxic and Hazardous Substances, standard number: 1910.1048, App A 2013a. https://www.osha.gov/pls/oshaweb/owadisp.show_document?p_id=10076&p_table=standards. Acessed Apr 2019

  • Paoli L, Maccelli C, Guarnieri M, Vannini A, Loppi S (2019) Lichens “travelling” in smokers’ cars are suitable biomonitors of indoor air quality. Ecol Indic 103:576–580. https://doi.org/10.1016/j.ecolind.2019.04.058

    Article  CAS  Google Scholar 

  • Parthasarathy S, Maddalena RL, Russell ML, Apte MG (2011) Effect of temperature and humidity on formaldehyde emissions in temporary housing units. J Air Waste Manage Assoc 6:689–695. https://doi.org/10.3155/1047-3289.61.6.689

    Article  CAS  Google Scholar 

  • Pereira EC, Santos LP, Silva AKO, Silva RF, Silva NH, Buril MLL, Martins MCB, Santiago R, Vicente C, Legaz ME (2019a) Interaction of Cladoniaceae lichens with Quartzarenic Neosols in Northeastern Brazil: a mini review. Revista Brasileira de Geografia Física 12:2302–2312. https://doi.org/10.26848/rbgf.v12.6.p2302-2312

    Article  Google Scholar 

  • Pereira N, Cardozo MV, Rocha TAS, Zero RC, Ávila FA, Oliveira FS (2019b) Microbiological analysis in the fixation and preservation of dog cadavers with ethyl alcohol and sodium chloride solution. Semina: Ciênc Agrár. https://doi.org/10.5433/1679-0359.2019v40n6supl2p3099

  • Piccotto M, Tretiach M (2010) Photosynthesis in chlorolichens: the influence of the habitat light regime. J Plant Res 123:763–775. https://doi.org/10.1007/s10265-010-0329-2

    Article  CAS  Google Scholar 

  • Pilegaard K (1978) Airborne metals and SO2 monitored by epiphytic lichens in an industrial area. Environ Pollut 17:81–92. https://doi.org/10.1016/0013-9327(78)90042-3

    Article  CAS  Google Scholar 

  • Pinheiro HLC, Andrade MV, Pereira PAP, Andrade JB (2004) Spectrofluorimetric determination of formaldehyde in air after collection onto silica cartridges coated with Fluoral P. Microchem J 78:15–20. https://doi.org/10.1016/j.microc.2004.02.017

    Article  CAS  Google Scholar 

  • Pompelli MF, França SC, Tigre RF, Oliveira MT, Sacilot M, Pereira EC (2013) Spectrophotometric determinations of chloroplastidic pigments in acetone, ethanol and dimethylsulphoxide. Braz J Biosci 11:52–58 http://www.ufrgs.br/seerbio/ojs/index.php/rbb/article/viewFile/2281/1180

    Google Scholar 

  • Rai A (1990) CRC Handbook of Symbiotic Cyanobacteria. CRC Press, Boca Raton. https://doi.org/10.1201/9781351071185

    Book  Google Scholar 

  • Salthammer T, Giesen R, Schripp T (2017) A permeation-controlled formaldehyde reference source for application in environmental test chambers. Chemosphere. 184:900–906. https://doi.org/10.1016/j.chemosphere.2017.06.057

    Article  CAS  Google Scholar 

  • Saowakon N, Ngernsoungnern P, Watcharavitoon P, Ngernsoungnern A, Kosanlavit R (2015) Formaldehyde exposure in gross anatomy laboratory of Suranaree University of Technology: a comparison of area and personal sampling. Environ Sci Pollut Res 22:19002–19012. https://doi.org/10.1007/s11356-015-5078-2

    Article  CAS  Google Scholar 

  • Silva RA (2002) Cladonia verticillaris (líquen) como biomonitor padrão da qualidade do ar no Distrito de Jaboatão-PE. Dissertation, Universidade Federal de Pernambuco

  • Silva AKO, Pereira IMC, Silva N, Mota-Filho FO, Pereira ECG (2014) Líquens utilizados como biomonitores da qualidade do ar no parque da Jaqueira -Recife-Pernambuco. Geo UERJ. https://doi.org/10.12957/geouerj.2014.5690

  • Su C, Ming H, Yang Y, Ma W, Li H, Li L (2019) Estimates of parameters for formaldehyde emission model from plywood panel under various temperature and relative humidity conditions. J Environ Sci Health A 54:48–55. https://doi.org/10.1080/10934529.2018.1511363

    Article  CAS  Google Scholar 

  • Tamayo AL, Alzate GA (2018) Preservation of animal cadavers with a formaldehyde-free solution for gross anatomy. J Morphol Sci 35:136–141. https://doi.org/10.1055/s-0038-1669434

    Article  Google Scholar 

  • USEPA – United States Environmental Protection Agency (1989) Risk assessment guidance for superfund, Vol I, human health evaluation manual (part A)

  • USEPA – United States Environmental Protection Agency (1992) Guidelines for exposure assessment. Office of Research Development, Office of Health and Environmental Assessment, Washington, DC

    Google Scholar 

  • USEPA – United States Environmental Protection Agency (1996) Risk assessment guidance for superfund (RAGS) Part A: Chapter 7 (toxicity assessment) and 8 (risk characterisation)

  • USEPA – United States Environmental Protection Agency (1997) Exposure factors handbook. US Government Printing Office, Washington, DC

    Google Scholar 

  • USEPA – United States Environmental Protection Agency (2001) Risk Assessment Guidance for Superfund (RAGS) Volume III - Part A: Process for Conducting Probabilistic Risk Assessment, Appendix B. Office of Emergency and Remedial Response, v. III, n. December, p. 1–385

  • USEPA – United States Environmental Protection Agency (2004) Integrated risk information system. www.epa.gov/iris. Acessed Apr 2019

  • Vasconcelos TL, Armas R, Pereira EC, Santiago R, Silva NH, Vicente C, Legaz ME (2016) Effects of both urea and light on the ability of accumulation and secretion of proteins and phenolics by Cladonia verticillaris. J Soil Sci Res 1:32–41

    Google Scholar 

  • Vernon LP (1960) Spectrophotometric determination of chlorophylls and pheophytins in plant extracts. Anal Chem 32:1144–1150. https://doi.org/10.1021/ac60165a029

    Article  CAS  Google Scholar 

  • Vicente C, Solas MT, Pereyra MT, Pereira EC, Pedrosa M (1995) Immobilisation of lichen cells and enzymes for bioproduction of lichen metabolites: technical requirements and optimisation of product recovering. Geobotanical and Phytotaxonomical Study Group, Botanical Institute, University of Cologne, Cologne, pp 97–110

    Google Scholar 

  • Viegas S, Prista J (2009) Exposição profissional a formaldeído – que realidade em Portugal? Rev Sci Saúde Tecnol 4:46–53. https://doi.org/10.25758/set.294

    Article  Google Scholar 

  • Villarouco FMO, Freire EVC, Pereira ECG, Perez REU (2007) Analysis of the lichen Cladonia verticillaris (Raddi) Fr., in laboratory conditions under styrene and ciclohexane effect. Interciência 32:242–246

    Google Scholar 

  • Vimercati L, Carrus A, Martino T, Galise I, Minunni V, Caputo F, Assennato G (2010) Formaldehyde exposure and irritative effects on medical examiners, pathologic anatomy post-graduate students and technicians. Iran J Public Health 39:26–34

    CAS  Google Scholar 

  • Vohra MS (2011) Personal formaldehyde exposure level in the gross anatomy dissecting room at College of Medicine King Saud University Riyadh. Int J Occup Med Environ Health 24:108–113. https://doi.org/10.2478/s13382-011-0004-4

    Article  Google Scholar 

  • Yatawara M, Dayananda (2019) Use of corticolous lichens for the assessment of ambient air quality along rural–urban ecosystems of tropics: a study in Sri Lanka. Environ Monit Assess 191:179. https://doi.org/10.1007/s10661-019-7334-2

    Article  CAS  Google Scholar 

  • Zhang L, Freeman L, Beane N, Jun H, Stephen SV, John JS, Martyn TS, Babasaheb RH, Chapel C (2010) Formaldehyde and leukemia: epidemiology, potential mechanisms, and implications for risk assessment Luoping. Environ Mol Mutagen. https://doi.org/10.1002/em.20534

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Acknowledgements

The authors thank at Dr. Ana Barbara Freitas Godinho, responsable by Morphology and Animal Pathology laboratory of the Darcy Ribeiro North Fluminense State University This work was supported by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, Brasil (CAPES), finance code 001, and the Conselho Nacional de Desenvolvimento Científico e Tecnológico, Brasil (CNPQ) (303285/2019-2).

Funding

This study is funded by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, Brasil (CAPES), finance code 001, and the Conselho Nacional de Desenvolvimento Científico e Tecnológico, Brasil (CNPQ) (303285/2019-2).

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Authors and Affiliations

  1. Grupo de Pesquisa em Química Ambiental (GPQA) - Universidade Estadual do Norte Fluminense Darcy Ribeiro, Avenida Alberto Lamego, 2000, 28013-602, Campos dos Goytacazes, Rio de Janeiro, Brasil

    Izabela Gonçalves da Silva & Maria Cristina Canela

  2. Instituto Federal de Educação, Ciência e Tecnologia Fluminense, Itaperuna, Rio de Janeiro, Brasil

    Camila Ramos de Oliveira Nunes

  3. Instituto Federal de Educação, Ciência e Tecnologia Fluminense, Campos dos Goytacazes, Rio de Janeiro, Brasil

    Rafael de Oliveira Costa

  4. Departamento de Ciências Geográficas, Universidade Federal de Pernambuco, Recife, Pernambuco, Brasil

    Eugênia Cristina Pereira

Authors
  1. Izabela Gonçalves da Silva
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  2. Camila Ramos de Oliveira Nunes
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  3. Rafael de Oliveira Costa
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  4. Eugênia Cristina Pereira
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  5. Maria Cristina Canela
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Contributions

IGS was responsible by the investigation performed the sampling, analysis, and data treatment, and contributes to conceptualization and writing the original draft and review the manuscript. CRON was responsible for performing the validation of the formaldehyde analysis and sampling. RMC contributes to the lichen experimental and analysis. ECP was responsible for the conceptualization of the lichen experimental, discussions and collected lichens for this study. ECP has also contributed for the review of this manuscript. MCC was responsible for the conceptualization, funding acquisition, project administration, resources, supervision and writing the original draft, and review and editing of this manuscript.

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Correspondence to Maria Cristina Canela.

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Formaldehyde concentration in the anatomy laboratory has cancer risk for the occupants and caused the changes in the lichen Cladonia verticillaris.

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da Silva, I.G., de Oliveira Nunes, C.R., de Oliveira Costa, R. et al. Formaldehyde exposure and atmospheric biomonitoring with lichen Cladonia verticillaris in an anatomy laboratory. Environ Sci Pollut Res 28, 48569–48580 (2021). https://doi.org/10.1007/s11356-021-14036-9

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