Indicator organism

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Indicator organisms are used as a proxy to monitor conditions in a particular environment, ecosystem, area, habitat, or consumer product. Certain bacteria, fungi and helminth eggs are being used for various purposes.

Contents

Types

Indicator bacteria

Certain bacteria can be used as indicator organisms in particular situations, such as when present in bodies of water. Indicator bacteria themselves may not be pathogenic but their presence in waste may indicate the presence of other pathogens. [1] Similar to how there are various types of indicator organisms, there are also various types of indicator bacteria. The most common indicators are total coliforms, fecal coliforms, E. coli, and enterococci. [2] The presence of bacteria commonly found in human feces, termed coliform bacteria (e.g. E. coli ), in surface water is a common indicator of faecal contamination. The means by which pathogens found in fecal matter can enter recreational bodies of water include, but are not limited to, sewage, septic systems, urban runoff, coastal recreational waste, and livestock waste. [2]

For this reason, sanitation programs often test water for the presence of these organisms to ensure that drinking water systems are not contaminated with feces. This testing can be done using several methods which generally involve taking samples of water, or passing large amounts of water through a filter to sample bacteria, then testing to see if bacteria from that water grow on selective media such as MacConkey agar. MacConkey agar will only allow the growth of gram-negative bacteria and the bacteria will grow differently according to how it metabolizes lactose or its lack of ability to metabolize it. [3] Alternatively, the sample can be tested to see if it utilizes various nutrients in ways characteristic of coliform bacteria. [4]

Coliform bacteria selected as indicators of faecal contamination must not persist in the environment for long periods of time following efflux from the intestine, and their presence must be closely correlated with contamination by other faecal organisms. Indicator organisms need not be pathogenic. [5]

Non-coliform bacteria, such as Streptococcus bovis and certain clostridia, may also be used as an index of faecal contamination. [6]

The presence of indicator bacteria is measured in a variety of ecosystems and sometimes alongside other measurements. In the Great Lakes, a study was conducted testing for both fecal indicator bacteria (FIB) concentrations and pathogen gene markers. [7] The FIB measured in this study included fecal coliform bacteria, E. coli, and enterococci. [7] FIB were collected via membrane filtration and serial dilution methods, producing samples which could be cultured and used to run PCR and amplify the pathogenic genes in question. [7] Among the 22 sampling locations, 165 samples were analyzed and E. coli concentrations were found to range from less than 2 to 26,000 CFU/100mL, enterococci ranged from less than 2 to 31,000 CFU/100mL, and fecal coliform bacteria ranged from less than 2 to 950 CFU/100mL. [7]

Another example of indicator bacteria being measured for safety purposes is in Malibu, CA. The state of California requires that beaches with greater than 50,000 visitors a year be monitored for FIB. [8] High FIB concentrations, exceeding what is considered acceptable by the EPA were observed in Malibu Lagoon and other Malibu beaches. [8] Measurement of high levels of FIB leads to a search to determine what the source(s) is/are. Potential sources of FIB in the Malibu area include waste from sewage treatment systems, runoff from local developments, and wildlife waste. [8] Common FIB were measured including enterococci which presented itself in levels as high as 242,000 MPN/100mL within onsite wastewater treatment systems. [8] The measurement of FIB is widespread and used for the purpose of providing safe waters.

In Texas, the occurrence and distribution of FIB, in particular fecal coliforms and E. coli, were measured in streams that receive discharge from the Dallas Fort Worth International Airport and the surrounding area. [9] These streams receiving the waste are home to aquatic life, used for recreational purposes, and as fishing sites. [9] Various standards exist in order to ensure the safety of all organisms present in the ecosystem, including humans. E. coli is used as an indicator of unsafe or below standard water quality for recreational use in Texas. [10] The standards for E. coli levels that declare contact recreation unsafe are a geometric mean of over 126 cfu/100mL or over a fourth of the samples measuring levels greater than 394cfu/100mL. [10] Various sites were tested, some found to exceed acceptable levels of E. coli and therefore did not support recreational use. [9] This is yet another example of how testing for indicator bacteria is used to determine whether bodies of water are safe for various uses, particularly recreational use.

Indicator fungi

Penicillium species, Aspergillus niger and Candida albicans are used in the pharmaceutical industry for microbial limit testing, bioburden assessment, method validation, antimicrobial challenge tests, and quality control testing. [11] When used in this capacity, Penicillium and A. niger are compendial mold indicator organisms. [11]

Molds such as Trichoderma , Exophiala , Stachybotrys , Aspergillus fumigatus , Aspergillus versicolor , Phialophora , Fusarium , Ulocladium and certain yeasts are used as indicators of indoor air quality. [12] [13] [14]

Metagenomic techniques allow for the sequencing of whole populations of microorganisms in a single operation.  With metagenomic sequencing, it is possible to use the entire community of fungal organisms, or mycobiome in the soil or water of a given area as a biological indicator [15] of anthropogenic activity, such as sewage overflow from an urban area or fertilizer and pesticide runoff from an agricultural one.

Composition of fungal communities has been found to be a good indicator of environmental properties like pH, altitude and water temperature. Chauvet [16] used this approach to take ecosystem-wide measurements of these variables using a network of monitoring stations at 27 streams in Southwestern France.

Cudowski et al. [17] sampled fungi in the water of the Augustow canal in eastern Poland. They took many standard measures of water quality -- temperature, oxygen saturation, pH, and dissolved nitrogen, organic carbon and sulfur levels. They identified species with microscopic methods and RFLP analysis. They found 38 fungal species, including 12 hyphomycetiae and 13 potential pathogens, belonging either to the dermatophytes or to relatives of C. albicans.  Cudowski et al. found that they could determine whether a sample of water had been taken from the natural (lake-like) or artificial part of the canal. They also found that the three major groups of fungi that they found, hyphomycetes, dermatophytes and Candida relatives, could predict many of their water quality measurements, which formed two clusters in a redundancy analysis.

Bouffand et al. [18] used Arbuscular Mycorhizzal Fungi (AMF), an asexual clade of fungi that form symbiotic relationships with plant root systems, as indicators to assess soil function and biodiversity in many sites across Europe.  They took soil samples in various climatic zones (atlantic, continental, mediterranean, alpine) and three land use regimes (arable, grassland, forestry), and sequenced the DNA of the fungi the soil contained. They found eight indicator species for soil pH: four that were only present when pH was less than 5, three for pH > 5 and one for pH > 7.  They found eight indicators of land use: two for forests, five for farm- and grassland, and one for both.  They also found one indicator fungus that was present when soil organic carbon was high, and another present when it was low.

Indicator helminth eggs

Identification and quantification of helminth eggs at UNAM university in Mexico City, Mexico Identification and quantification of helminth eggs.png
Identification and quantification of helminth eggs at UNAM university in Mexico City, Mexico

The eggs from helminths (parasitic worms) are a commonly used indicator organism to assess the safety of sanitation and wastewater reuse systems (such schemes are also called reuse of human excreta). [19] : 55  This is because they are the most resistant pathogens of all types of pathogens (pathogens can be viruses, bacteria, protozoa and helminths). [20] It means they are relatively hard to destroy through conventional treatment methods. They can survive for 10–12 months in tropical climates. [20] These eggs are also called ova in the literature. [21]

Helminth eggs that are found in wastewater and sludge stem from soil-transmitted helminths (STHs) which include Ascaris lumbricoides (Ascaris), Anclostoma duodenale , Necator americanus (hookworm), and Trichuris trichiura (whipworm). [22] Ascaris and whipworm that are identified in reusable wastewater systems can cause certain diseases and complications if ingested by humans and pigs. [23] Hookworms will plant and hatch their larvae into the soil where they grow until maturity. Once the hookworm eggs are fully developed, they infect organisms by crawling through the organism’s skin. [24]

The presence or absence of viable helminth eggs ("viable" meaning that a larva would be able to hatch from the egg) in a sample of dried fecal matter, compost or fecal sludge is often used to assess the efficiency of diverse wastewater and sludge treatment processes in terms of pathogen removal. [19] : 55  In particular, the number of viable Ascaris eggs is often taken as an indicator for all helminth eggs in treatment processes as they are very common in many parts of the world and relatively easy to identify under the microscope. However, the exact inactivation characteristics may vary for different types of helminth eggs. [25]

Various microscopic images of different types of helminth eggs Collage of various helminth eggs.png
Various microscopic images of different types of helminth eggs

The technique used for testing depends on the type of sample. [21] When the helminth ova are in sludge, processes such as alkaline-post stabilization, acid treatment, and anaerobic digestion are used to reduce the amount of helminth ova in areas where there is a large amount. These methods make it possible for helminth ova to be within the healthy requirements of ≤1 helminth ova per liter. Dehydration is used to inactivate helminth ova in fecal sludge. This type of inactivation occurs when feces is stored between 1-2 years, a high total solids content (>50-60%) is present, items such as leaves, lime, earth, etc. are added, and at a temperature of 30°C or higher. [24]

See also

Related Research Articles

<span class="mw-page-title-main">Sanitation</span> Public health conditions related to clean water and proper excreta and sewage disposal

Sanitation refers to public health conditions related to clean drinking water and treatment and disposal of human excreta and sewage. Preventing human contact with feces is part of sanitation, as is hand washing with soap. Sanitation systems aim to protect human health by providing a clean environment that will stop the transmission of disease, especially through the fecal–oral route. For example, diarrhea, a main cause of malnutrition and stunted growth in children, can be reduced through adequate sanitation. There are many other diseases which are easily transmitted in communities that have low levels of sanitation, such as ascariasis, cholera, hepatitis, polio, schistosomiasis, and trachoma, to name just a few.

<i>Enterococcus</i> Genus of bacteria

Enterococcus is a large genus of lactic acid bacteria of the phylum Bacillota. Enterococci are Gram-positive cocci that often occur in pairs (diplococci) or short chains, and are difficult to distinguish from streptococci on physical characteristics alone. Two species are common commensal organisms in the intestines of humans: E. faecalis (90–95%) and E. faecium (5–10%). Rare clusters of infections occur with other species, including E. casseliflavus, E. gallinarum, and E. raffinosus.

<span class="mw-page-title-main">Septic tank</span> Method for basic wastewater treatment (on-site)

A septic tank is an underground chamber made of concrete, fiberglass, or plastic through which domestic wastewater (sewage) flows for basic sewage treatment. Settling and anaerobic digestion processes reduce solids and organics, but the treatment efficiency is only moderate. Septic tank systems are a type of simple onsite sewage facility. They can be used in areas that are not connected to a sewerage system, such as rural areas. The treated liquid effluent is commonly disposed in a septic drain field, which provides further treatment. Nonetheless, groundwater pollution may occur and is a problem.

<span class="mw-page-title-main">Bacteriological water analysis</span> Method of analysing water

Bacteriological water analysis is a method of analysing water to estimate the numbers of bacteria present and, if needed, to find out what sort of bacteria they are. It represents one aspect of water quality. It is a microbiological analytical procedure which uses samples of water and from these samples determines the concentration of bacteria. It is then possible to draw inferences about the suitability of the water for use from these concentrations. This process is used, for example, to routinely confirm that water is safe for human consumption or that bathing and recreational waters are safe to use.

<span class="mw-page-title-main">Biosolids</span> Decontaminated sewage sludge

Biosolids are solid organic matter recovered from a sewage treatment process and used as fertilizer. In the past, it was common for farmers to use animal manure to improve their soil fertility. In the 1920s, the farming community began also to use sewage sludge from local wastewater treatment plants. Scientific research over many years has confirmed that these biosolids contain similar nutrients to those in animal manures. Biosolids that are used as fertilizer in farming are usually treated to help to prevent disease-causing pathogens from spreading to the public. Some sewage sludge can not qualify as biosolids due to persistent, bioaccumulative and toxic chemicals, radionuclides, and heavy metals at levels sufficient to contaminate soil and water when applied to land.

<span class="mw-page-title-main">Waste stabilization pond</span> Ponds designed and built for wastewater treatment

Waste stabilization ponds are ponds designed and built for wastewater treatment to reduce the organic content and remove pathogens from wastewater. They are man-made depressions confined by earthen structures. Wastewater or "influent" enters on one side of the waste stabilization pond and exits on the other side as "effluent", after spending several days in the pond, during which treatment processes take place.

<span class="mw-page-title-main">Coliform bacteria</span> Group of bacterial species

Coliform bacteria are defined as either motile or non-motile Gram-negative non-spore forming bacilli that possess β-galactosidase to produce acids and gases under their optimal growth temperature of 35–37 °C. They can be aerobes or facultative aerobes, and are a commonly used indicator of low sanitary quality of foods, milk, and water. Coliforms can be found in the aquatic environment, in soil and on vegetation; they are universally present in large numbers in the feces of warm-blooded animals as they are known to inhabit the gastrointestinal system. While coliform bacteria are not normally the cause of serious illness, they are easy to culture, and their presence is used to infer that other pathogenic organisms of fecal origin may be present in a sample, or that said sample is not safe to consume. Such pathogens include disease-causing bacteria, viruses, or protozoa and many multicellular parasites. Every drinking water source must be tested for the presence of these total coliform bacteria.

The coliform index is a rating of the purity of water based on a count of fecal bacteria. It is one of many tests done to assure sufficient water quality. Coliform bacteria are microorganisms that primarily originate in the intestines of warm-blooded animals. By testing for coliforms, especially the well known Escherichia coli, which is a thermotolerant coliform, one can determine if the water has possibly been exposed to fecal contamination; that is, whether it has come in contact with human or animal feces. It is important to know this because many disease-causing organisms are transferred from human and animal feces to water, from where they can be ingested by people and infect them. Water that has been contaminated by feces usually contains pathogenic bacteria, which can cause disease. Some types of coliforms cause disease, but the coliform index is primarily used to judge if other types of pathogenic bacteria are likely to be present in the water.

A fecal coliform is a facultatively anaerobic, rod-shaped, gram-negative, non-sporulating bacterium. Coliform bacteria generally originate in the intestines of warm-blooded animals. Fecal coliforms are capable of growth in the presence of bile salts or similar surface agents, are oxidase negative, and produce acid and gas from lactose within 48 hours at 44 ± 0.5°C. The term thermotolerant coliform is more correct and is gaining acceptance over "fecal coliform".

An anaerobic lagoon or manure lagoon is a man-made outdoor earthen basin filled with animal waste that undergoes anaerobic respiration as part of a system designed to manage and treat refuse created by concentrated animal feeding operations (CAFOs). Anaerobic lagoons are created from a manure slurry, which is washed out from underneath the animal pens and then piped into the lagoon. Sometimes the slurry is placed in an intermediate holding tank under or next to the barns before it is deposited in a lagoon. Once in the lagoon, the manure settles into two layers: a solid or sludge layer and a liquid layer. The manure then undergoes the process of anaerobic respiration, whereby the volatile organic compounds are converted into carbon dioxide and methane. Anaerobic lagoons are usually used to pretreat high strength industrial wastewaters and municipal wastewaters. This allows for preliminary sedimentation of suspended solids as a pretreatment process.

<span class="mw-page-title-main">Parasitic worm</span> Large type of parasitic organism

Parasitic worms, also known as helminths, are a polyphyletic group of large macroparasites; adults can generally be seen with the naked eye. Many are intestinal worms that are soil-transmitted and infect the gastrointestinal tract. Other parasitic worms such as schistosomes reside in blood vessels.

<span class="mw-page-title-main">Simmons' citrate agar</span> Differential culture medium

Simmons' citrate agar is used for differentiating gram-negative bacteria on the basis of citrate utilization, especially for distinguishing Gammaproteobacteria of the family Enterobacteriaceae or even between species of the same genus. For example, Salmonella enteritidis would yield a positive (blue) result on Simmons’ agar and thus be distinguished from other Salmonella species like Salmonella typhi, Salmonella pullorum, and Salmonella gallinarum, which would yield a negative (green) result.

Indicator bacteria are types of bacteria used to detect and estimate the level of fecal contamination of water. They are not dangerous to human health but are used to indicate the presence of a health risk.

<span class="mw-page-title-main">Petrifilm</span> Plating system

The Neogen Petrifilm plate is an all-in-one plating system made by the Food Safety Division of the Neogen Corporation. They are heavily used in many microbiology-related industries and fields to culture various micro-organisms and are meant to be a more efficient method for detection and enumeration compared to conventional plating techniques. A majority of its use is for the testing of foodstuffs.

<span class="mw-page-title-main">IMViC</span> Microbiological and biochemical method for identification

The IMViC tests are a group of individual tests used in microbiology lab testing to identify an organism in the coliform group. A coliform is a gram negative, aerobic, or facultative anaerobic rod, which produces gas from lactose within 48 hours. The presence of some coliforms indicate fecal contamination.

<span class="mw-page-title-main">Human feces</span> Metabolic waste of the human digestive system

Human feces or faeces British English), commonly and in medical literature more often called stool, are the solid or semisolid remains of food that could not be digested or absorbed in the small intestine of humans, but has been further broken down by bacteria in the large intestine. It also contains bacteria and a relatively small amount of metabolic waste products such as bacterially altered bilirubin, and the dead epithelial cells from the lining of the gut. It is discharged through the anus during a process called defecation.

<span class="mw-page-title-main">Sewage</span> Wastewater that is produced by a community of people

Sewage is a type of wastewater that is produced by a community of people. It is typically transported through a sewer system. Sewage consists of wastewater discharged from residences and from commercial, institutional and public facilities that exist in the locality. Sub-types of sewage are greywater and blackwater. Sewage also contains soaps and detergents. Food waste may be present from dishwashing, and food quantities may be increased where garbage disposal units are used. In regions where toilet paper is used rather than bidets, that paper is also added to the sewage. Sewage contains macro-pollutants and micro-pollutants, and may also incorporate some municipal solid waste and pollutants from industrial wastewater.

<span class="mw-page-title-main">Reuse of human excreta</span> Safe, beneficial use of human excreta mainly in agriculture (after treatment)

Reuse of human excreta is the safe, beneficial use of treated human excreta after applying suitable treatment steps and risk management approaches that are customized for the intended reuse application. Beneficial uses of the treated excreta may focus on using the plant-available nutrients that are contained in the treated excreta. They may also make use of the organic matter and energy contained in the excreta. To a lesser extent, reuse of the excreta's water content might also take place, although this is better known as water reclamation from municipal wastewater. The intended reuse applications for the nutrient content may include: soil conditioner or fertilizer in agriculture or horticultural activities. Other reuse applications, which focus more on the organic matter content of the excreta, include use as a fuel source or as an energy source in the form of biogas.

<span class="mw-page-title-main">Fecal sludge management</span> Collection, transport, and treatment of fecal sludge from onsite sanitation systems

Fecal sludge management (FSM) is the storage, collection, transport, treatment and safe end use or disposal of fecal sludge. Together, the collection, transport, treatment and end use of fecal sludge constitute the "value chain" or "service chain" of fecal sludge management. Fecal sludge is defined very broadly as what accumulates in onsite sanitation systems and specifically is not transported through a sewer. It is composed of human excreta, but also anything else that may go into an onsite containment technology, such as flushwater, cleansing materials, menstrual hygiene products, grey water, and solid waste. Fecal sludge that is removed from septic tanks is called septage.

<span class="mw-page-title-main">Pit additive</span> Material to reduce fecal sludge build-up

Pit additives is a commercially-produced material that aims to reduce fecal sludge build-up and control odor in pit latrines, septic tanks and wastewater treatment plants. Manufacturers claim to use effective microorganisms (EM) in their products. Current scientific evidence does not back up most claims made by manufacturers about the benefits. Removing sludge continues to be a problem in pit latrines and septic tanks.

References

  1. ↑ Noble, R.T; Moore, D.F; Leecaster, M.K; McGee, C.D; Weisberg, S.B (April 2003). "Comparison of total coliform, fecal coliform, and enterococcus bacterial indicator response for ocean recreational water quality testing". Water Research. 37 (7): 1637–1643. Bibcode:2003WatRe..37.1637N. doi:10.1016/s0043-1354(02)00496-7. ISSN   0043-1354. PMID   12600392.
  2. 1 2 Chapter 17: Bacteria Indicators of Potential Pathogens. Volunteer Estuary Monitoring: A Methods Manual. United States Environmental Protection Agency. 2006.
  3. ↑ Jung, Benjamin; Hoilat, Gilles J. (2021), "MacConkey Medium", StatPearls, Treasure Island (FL): StatPearls Publishing, PMID   32491326 , retrieved 26 April 2021
  4. ↑ Ashbolt NJ, Grabow WO, Snozzi M. "13: Indicators of microbial water quality". Assessing Microbial Safety of Drinking Water (PDF). World Health Organization. pp. 293–295. Retrieved 16 July 2016.
  5. ↑ "Fecal Coliform as an Indicator Organism" (PDF). Wastewater treatment environmental fact sheet. New Hampshire Department of Environmental Services. 2003. Retrieved 30 November 2007.
  6. ↑ Gerardi, Michael H.; Mel C. Zimmerman (January 2005). Michael H. Gerardi (ed.). Wastewater Pathogens. Wastewater Microbiology Series. Hoboken, NJ: John Wiley & Sons, Inc. p. 147. ISBN   978-0-471-20692-7.
  7. 1 2 3 4 Brennan, A. K., Johnson, H. E., Totten, A. R., Duris, J. W., Geological Survey (U.S.), & Great Lakes Restoration Initiative (U.S.). (2015). Occurrence and distribution of fecal indicator bacteria and gene markers of pathogenic bacteria in great lakes tributaries, march-october 2011 (Ser. Open-file report, 2015-1013). U.S. Department of the Interior, U.S. Geological Survey. https://permanent.fdlp.gov/gpo55630/ofr2015-1013.pdf
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  10. 1 2 Texas Commission on Environmental Quality, 2008a, 2000 Texas surface water quality standards: accessed November 4, 2008, at http://www.tceq.state.tx.us/permitting/water_ quality/wq_assessment/standards/WQ_standards_2000.html
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  12. ↑ Jantunen, Matti; Jaakkola, Jouni J. K.; Krzyzanowski, M., eds. (1997). "20: Bacteria and fungi". Assessment of Exposure to Indoor Air Pollutants, WHO Regional Publications European Series, No. 78. Copenhagen: WHO Regional Office Europe. pp. 101–102. ISBN   9289013427.
  13. ↑ Cole, Eugene C.; Dulaney, Pamela D.; Leese, Keith E.; Hall, Richard M.; Foarde, Karin K.; Franke, Deborah L.; Myers, Frank M.; Berry, Michael A. (1996). "Biopollutant Sampling and Analysis of Indoor Surface Dusts: Characterization of Potential Sources and Sinks". In Tichenor, Bruce A. (ed.). Characterizing Sources of Indoor Air Pollution and Related Sink Effects, Volume 1287. West Conshohocken, PA: ASTM International. p. 164. ISBN   9780803120303.
  14. ↑ Heikkinen, M.S.A.; Hjelmroos-Koski, M.K.; Haggblom, M.M.; Macher, J.M. (2004). "Chapter 13: Bioaerosols". In Ruzer, L.S.; Harley, N.H. (eds.). Aerosols Handbook: Measurement, Dosimetry, and Health Effects. Boca Raton, Florida: CRC Press. pp. 377–378. ISBN   9780203493182.
  15. ↑ Bai, Yaohui; Wang, Qiaojuan; Liao, Kailingli; Jian, Zhiyu; Zhao, Chen; Qu, Jiuhui (21 December 2018). "Fungal Community as a Bioindicator to Reflect Anthropogenic Activities in a River Ecosystem". Frontiers in Microbiology. 9: 3152. doi: 10.3389/fmicb.2018.03152 . ISSN   1664-302X. PMC   6308625 . PMID   30622523.
  16. ↑ Chauvet E, (1991). "Aquatic hyphomycete distribution in south-western France". Journal of Biogeography. 18: 699–706.
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  18. ↑ Bouffaud, Marie-Lara; Creamer, Rachel E.; Stone, Dote; Plassart, Pierre; Van Tuinen, Diederik; Lemanceau, Philippe; Wipf, Daniel; Redecker, Dirk (1 December 2016). "Indicator species and co-occurrence in communities of arbuscular mycorrhizal fungi at the European scale". Soil Biology and Biochemistry. 103: 464–470. Bibcode:2016SBiBi.103..464B. doi:10.1016/j.soilbio.2016.09.022. ISSN   0038-0717.
  19. 1 2 Von Sperling, M. (2015). "Wastewater Characteristics, Treatment and Disposal". Water Intelligence Online. 6: 9781780402086. doi: 10.2166/9781780402086 . ISSN   1476-1777.
  20. 1 2 Koné, Doulaye; Cofie, Olufunke; Zurbrügg, Christian; Gallizzi, Katharina; Moser, Daya; Drescher, Silke; Strauss, Martin (2007). "Helminth eggs inactivation efficiency by faecal sludge dewatering and co-composting in tropical climates". Water Research. 41 (19): 4397–4402. Bibcode:2007WatRe..41.4397K. doi:10.1016/j.watres.2007.06.024. PMID   17624391.
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  24. 1 2 Jiménez, B.; Maya, C.; Galván, M. (1 September 2007). "Helminth ova control in wastewater and sludge for advanced and conventional sanitation". Water Science and Technology. 56 (5): 43–51. Bibcode:2007WSTec..56...43J. doi: 10.2166/wst.2007.555 . ISSN   0273-1223. PMID   17881836.
  25. ↑ Maya C., Torner-Morales F.J., Lucario E.S., Hernández E., Jiménez B. (2012). "Viability of six species of larval and non-larval helminth eggs for different conditions of temperature, pH and dryness". Water Research. 46 (15): 4770–4782. Bibcode:2012WatRe..46.4770M. doi:10.1016/j.watres.2012.06.014. PMID   22794801.{{cite journal}}: CS1 maint: multiple names: authors list (link)

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