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Nevin S. Scrimshaw
Institute Professor, Massachusetts Institute of Technology, Cambridge, Massachusetts, USA, and Senior Adviser to the Rector, World Hunger Programme, the United Nations University
Experience with the attempted development of useful, safe, and commercially acceptable single-cell proteins products from petroleum hydrocarbon substrates gives an indication of the nature of the health problems and associated issues likely to be encountered in the development of biomass for similar purposes from plant and animal wastes Time after time, combinations of substrate, organisms, and processes that were demonstrated to be technologically feasible and economically viable have had to be abandoned because questions of safety arose that either required unacceptable added costs to eliminate hazards or resulted in regulatory or political obstacles impossible to surmount within economically feasible time limits.
From the beginning, fears were expressed that organisms selected, even if normally nontoxic, might undergo mutation to toxic strains or become contaminated by toxic strains. Concern also focused on the possible carry-over of toxic substances from substrates into single-cell products intended for direct human consumption, or into products for human consumption from animals fed these materials These concerns have proven extremely difficult to allay by the scientific method and have persisted long after extensive research has provided seemingly scientifically conclusive assurances. In Italy, neither British Petroleum (BP) nor Liquichimica was able to obtain authorization to operate plants already constructed, although in the judgement of the PAG and other experts all scientific questions had been answered satisfactorily (1).
In Japan, consumer alarm resulting primarily from an erroneous research report, exacerbated by unfortunate nomenclature, became a political issue and has blocked all efforts to produce single-cell protein from hydrocarbons in Japan even for animal feeding.
In addition to these issues, which, from a scientific point of view could be dealt with by extensive analytical procedures and by studies in a variety of experimental animals, problems arose that could not be predicted from the studies on experimental animals and proved, in some cases, to be of critical importance in determining feasibility. These were adverse organoleptic properties that could not be readily masked, and allergic reactions in some human subjects (2, 3). Sensitized individuals became susceptible to relatively small quantities and manifested cutaneous or gastro-intestinal symptoms at best unacceptable, and at worst, alarming and temporarily disabling. Because these were apparently caused by relatively small protein molecules, either present originally or resulting from nucleic acid reduction or other treatment, they could be removed by suitable processing procedures, but at significant additional cost.
Other health issues were also raised, often without any justification, but no less troublesome for this reason. It was suggested that working with live organisms could be hazardous to workers or to surrounding communities (perhaps an unconscious confusion with the escape of disease-producing organisms from the laboratory or publicized aspects of the controversy over the safety of DNA-recombinance research). The objection was also made that production of these materials might have other health-related environmental effects, ranging from atmospheric to thermal pollution. Problems with both added cost to the production of SCP on gas oil by BP in Lavera, France that tipped the balance against economic feasibility.
Based on these and other experiences and some of the additional information already presented, it is possible to develop a check list of health-related issues that might arise as a consequence of efforts to develop products involving microbial growth on vegetable and animal wastes (which the euphemism "residues" will not eliminate). I will refer to the primary material consisting of substrate plus a complex mixture of organisms as MBP (microbial biomass product). Table 1 lists the assurances necessary for application of microbiological techniques to the use of plant and animal residues for the production of either MBP or SCP for animal or human consumption.
TABLE 1. Assurances Necessary for Application of Microbial Techniques to Organic Residues for Either Animal or Human Feeding
1. Regulatory approval
2. Economic feasibility
3. Environmental acceptability
a) aesthetic issues
b) health issues
4. Favourable political climate
For animal rations, and of course also for human feeding, there must be assurance that the species of organisms involved are in themselves non-toxic. Even when a given organism under one set of conditions can be demonstrated to be nontoxic in acute feeding trials at high levels, fear of harmful mutations will persist, especially if other strains of the species or of closely related species are known to be toxic. Where mixed cultures under non-sterile conditions are involved, as in practical village level fermentations, there will be concern not only for the possibility of toxic species developing under some circumstances, but also that pathogenic species may become accidental contaminants (Table 2). The former (toxicity of the primary organisms) must be answered by either experimental or practical feeding studies, and the latter (introduction of pathogens) by the necessary precautions and conditions.
TABLE 2. Health Aspects of Biomass from Organic Residues
Safety of species
(a) of primary organisms
(b) of usual contaminating organisms
(c) possibility of accidental introduction of pathogenic species
(e.g., botulism, salmonellosis)
The problem of mycotoxins requires special consideration because they may be introduced by vegetable substrates on which there has been prior growth of a toxin-producing mould, especially Aspergillus flavus. It is possible that mycotoxin levels unassociated with signs of toxicity in practical feeding of animals may result in mycotoxins in the food product, milk being the prototype example.
The very heterogeneous substrates provided by waste materials raise many questions. These include the possible accumulation of unacceptable concentrations of such heavy metals as lead, mercury, copper, zinc, arsenic, cadmium, and cobalt, and of insecticides, herbicides, larvicides, and other toxic chemicals. Toxic metabolites are always a theoretical possibility, and elimination of foreign bodies may be a problem (Table 3).
TABLE 3. Health Aspects of Substrates Used for Microbial Conversion of Organic Residues
Safety of substrates
(a) pathogens
(b) heavy metals (Hg, Cu. Cd, Pb, Al, As)
(c) pesticide residues
(d) drug residues
(e) toxic metabolites
(f) foreign bodies
Even when it can be shown that the proposed biomass (either MBP or SCP) produces excellent results in experimental and practical animal feeding, the lives of food animals are relatively short and their growth may not reflect the effects of residual compounds that could, in theory, have adverse consequences in long-term use by human subjects. For example, Toprina and Liquipron are the trade names for yeast grown on petroleumhydrocarbon substrates and proposed for commercial production in Italy. It was necessary to prove that the odd-numbered carbon-chain fatty acids seen in the fat of animals fed Toprina or Liquipton were naturally occurring compounds metabolized normally through usual biochemical pathways (4). It was also established that cell function of the various tissues was unaffected by the presence of odd-numbered carbon-chain fatty acids even when they were present in relatively large amounts (e.g., ref. 1, 5). Similar questions might be asked regarding the edible products of animals fed on MBP.
Sometimes a substrate can increase the likelihood of disease transmission when an animal product is improperly processed or handled; for example, an increased risk of salmonellosis. Fish grown in a pond contaminated with raw sewage may introduce pathogens into the environment even when the cooked fish is quite safe. In theory also, the use of plant residues could result in the appearance of plant steroid hormones in unacceptable amounts in animal products, but to my knowledge, this has never been reported except from direct consumption of certain plant species.
Obviously, the MBP must have an acceptable nutritional value for animal feeding and not cause unacceptable flavours in the resulting products.
For direct human use, these products must not only satisfy all of the conditions for animal feeding, but also a series of additional criteria. It must be established that there is no possibility of consuming, in the products of animals fed MBP, substances that might be mutagenic or carcinogenic in prolonged human feeding, or teratogenic when fed to women during early pregnancy. It is not practical to determine this by human feeding studies, but rather by appropriately designed multi-generational and reproductive studies in experimental animals.
Of more practical significance is the possibility that feeding the material directly to humans may cause cutaneous or gastrointestinal responses of an allergic nature in an unacceptable proportion of human subjects. This must be detected in advance by well designed double-blind feeding trials in a sufficiently large sample of human subjects for at least 30 days. Because occasional allergic responses will be found to all protein foods, particularly common with peanuts, milk, and eggs, absolute freedom from allergenicity cannot be expected.
MBP for human consumption must also have favourable organoleptic characteristics or functional properties, or both, that favour its use.
The social and anthropological considerations associated with SCP and MBP heavily overlap, but are far from identical with the health considerations. Concerns of the public and of politicians are usually expressed in health terms, although in some cases objections have been aesthetic in nature with no scientific basis. At the village level, concepts of acceptable practices are culture-specific, and extrapolations from the attitudes of one culture to those of another must be avoided. For example, latrines built over fish ponds to admit human faeces directly into the water are used effectively in some cultures but would be totally unacceptable in others. Obviously, orthodox Muslims would not accept an integrated scheme for swine and algae production.
Cultural obstacles may also be subtle and unrecognized by outside planners and organizers until the reasons for failure of a seemingly feasible programme are examined in depth. Cultural resistance to a village-level project may not be due to concerns about the process or product itself, but rather the proposed method of introduction may not fit the social practices of the village. For example, the proposal may require men to play a role that is traditionally for women, or depend on new, difficult-to-introduce patterns of social or economic co-operation among families. If it undermines traditional authority patterns in a village, strong resistance may be encountered.
The time to determine social and cultural attitudes and barriers is before a programme is formulated or announced. Such investigations can lead to the conclusion that a project should not be attempted, but it is to be hoped that they will also indicate approaches that will give a proposed project a better chance of success.
Whether animal or human feeding is the intended use for an MBP, certain problems will be common to both, and, as listed in Table 4, these are directly or indirectly health-related. In many countries, MBP, like SCP projects, may require regulatory approval. Economic feasibility is, of course, essential and will depend, in part, on the attitude of regulatory authorities and the potential consumer. MBP products will also be vulnerable to environmental costs and environmental acceptability. These include concern for possible adverse effects on water quality, including increased BOD, water-borne infections, infectious disease vectors in water, pollution with heavy metals and pesticides, or undesirable odours and tastes. Competition for alternate uses of land or water may also be a consideration.
TABLE 4 Assurances Necessary for Application of Microbiological Techniques to Organic Residues
For animal use
(a) safety of species
(b) safety of substrates
(c) safety of animal products
(d) nutritional value
For human use (additional considerations)
(e) lack of allergenicity
(f) lack of mutagenicity/carcinogenicity
(g) lack of teratogenicity
(h) favourable organoleptic or functional characteristics
(i) cultural acceptability
All of the above may be factors in determining whether the political climate will be favourable to, or at least not in opposition to, specific MBP or SCP development. This will, in turn, be heavily influenced by perceived health risks and benefits of the kinds mentioned above, whether or not these are real or imaginary.
Governments and the public tend to be frightened by possible new hazards introduced by science and technology, and strangely complacent about existing ones of far greater magnitude. Given the importance of ensuring favourable attitudes on the part of politicians and the public, it will be important to avoid some of the mistakes made in hydrocarbon-SCP development and to try to assure positive attitudes towards the safety, nutritional value, and usefulness of MBP.
As already suggested, nomenclature may play a significant role in public perception of health considerations. Single-cell protein is not a scientifically accurate term, because all protein comes from single cells, but it was selected in my office at MIT and introduced as the title of the first conference on proteins from yeast and bacteria, held at MIT in 1967. It was chosen in preference to "microbial protein" and other names that already had negative connotations. The term "SCP" has been applied to describe the biomass consisting entirely of the cells of a single organism, or a limited number of species, produced on relatively pure substrates. Needless to say, it met a need and came rapidly into world-wide use. It is now proposed that we apply the new acronym MOP (for microbial biomass product) to the complex mixture of substrate and micro-organisms produced by the fermentation of unrefined animal and vegetable wastes. It is obviously intended to complement the term SCP and to avoid the use of the latter when referring to the complex combinations of substrate and micro-organisms that are the main concerns of this workshop.
It seems likely that the production of biomass for human consumption from carbohydrate rather than from hydrocarbon substrates will continue to fall mainly in the category of SCP, where safety of substrates and organisms can be assured by animal and human testing and careful controls. However, these are not usually produced by village-level processes, much less household ones. There is one category of MBP that might readily be developed for human consumption, utilizing substrates that are already edible and need merely to be upgraded organoleptically, functionally, or nutritionally by the microbiological process, This is the basis of such traditional foods as tempeh, ontjom, and bongkrek, already mentioned by Steinkraus at this workshop (6). It is entirely possible that more such foods can be developed, but each will either be an outgrowth of traditional practices confirmed by usage, or will require the kind of preclinical and clinical testing described in PAG Guidelines 6, 7, and 12 (7 - 9).
1. S. Garattini, S. Paglialunga, and N.S. Scrimshaw, (eds.), Single-Cell Protein - Safety for Animal and Human Feeding, Pergamon Press, Oxford and New York, 1979.
2. E.J. Eastham, "Clinical Gastro-Intestinal Allergy," in S. Garattini, S. Paglialunga, and N.S. Scrimshaw, (eds.), Single-Cell Protein-Safety for Animal and Human Feeding, Pergamon Press, Oxford and New York, 1979.
3. N.S. Scrimshaw, "Allergic Responses to Some Single-Cell Proteins in Human Subjects," in S. Garattini, S. Paglialunga, and N.S. Scrimshaw, (eds.), Single-Cell Protein - Safety for Animal and Human Feeding, Pergamon Press, Oxford and New York, 1979.
4. C.A. Shacklady, "e-Paraffins in Tissues of Animals Fed on Alkane-Grown Yeasts," in S. Garattini, S. Paglialunga, and N.S. Scrimshaw, (eds.), Single-Cell Protein - Safety for Animal and Human Feeding, Pergamon Press, Oxford and New York, 1979.
5. S.R. Tannenbausm and D.I.C. Wang, (eds.), Single-Cell Protein - 11, MIT Press, Cambridge, Massachusetts, 1975.
6. K.H. Steinkraus, "Production of Microbial Protein Foods on Edible Substrates, Food Byproducts, and Ligno-Cellulosic Wastes," pp. 41 - 46, these proceedings.
7. Protein-Calorie Advisory Group of the United Nations System (PAG) Guideline No. 6, "Preclinical Testing of Novel Sources of Protein," United Nations, New York.
8. PAG Guideline No. 7, "Human Testing of Supplementary Food Mixtures," United Nations, New York.
9. PAG Guideline No. 12, ``Production of Single-Ceil Protein for Human Consumption," United Nations, New York.
In commenting on Scrimshaw's paper, La Rivière felt it necessary to record the effect of government actions upon factors affecting food production. The entire farming system in Western Europe and the United States depends on government subsidies to the extent that in the US some farmers have received subvention not to grow certain crops. Government subsidies might well be used to encourage the production of the bioconversion materials discussed in the papers at this conference.
The discussions closed with comments on the necessity of differentiating the qualities of energy in analyses of that factor. Although this is a complex evaluation, it is absolutely necessary if valid comparisons among different systems are to be obtained, a sine qua non for their practical application in rural communities.