Environmental Impact of Stratospheric Flight

BIOLOGICAL AND CLIMATIC EFFECTS OF AIRCRAFT EMISSIONS IN THE STRATOSPHERE

CLIMATIC IMPACT COMMITTEE

National Academy of Sciences

National Academy of Engineering

NATIONAL ACADEMY OF SCIENCES

WASHINGTON, D.C. 1975

3

Biological and Medical Effects of Nitrogen Oxide Emissions

I. Introduction

It is shown in the previous chapter that the addition of NOx to the stratosphere from aircraft engines or other sources can reduce the total ozone column density with a consequent increase in the intensity of solar ultraviolet (uv) radiation reaching the earth's surface. This chapter addresses the question of whether an increase in ultraviolet flux can pose a problem to the human population, to agriculture, or to any other part of the biosphere.

II. Sun Exposure and Man

Although people have recognized that they should take precautions against painful sunburn, depending on their particular susceptibility, there has been a general belief that sunlight is one of the gifts from nature. The danger of excessive sun exposure is a subject that has only recently received considerable attention. It is now virtually certain that there are a number of negative long-term effects of sun exposure.

There is no immediate warning signal of inadvertent uv exposure such as occurs with a heat burn. It is surreptitious and invisible, and reaction to it is delayed (even sunburn is a delayed reaction). There is strong evidence that damage is cumulative--the older a person is the more damage he has. Increased exposure to uv is known to increase the rate of skin aging. As one dermatologist put it, "the beaches are filled today with people seeking to improve or maintain those highly coveted dark golden tans--unknowingly they are building elephant skin for their later years." Only recently have there been public warnings that excessive exposure to sunlight can cause skin cancer.

The major known direct effects of the sun's uv radiation are on the skin and eyes, because uv radiation will not penetrate deeper than the skin itself (see CIAP Monograph 5, Chapter 3.5). At short wavelengths little uv radiation penetrates the ozone layer; at long wavelengths the skin is relatively insensitive. The damage comes from a narrow band of the solar uv spectrum from 295 to 320 nm--a band whose intensity at the earth's surface is most altered by changes in stratospheric ozone concentration. This range nearly coincides with the 280-315-nm band for which the scientific shorthand is uv-B.

There are no quantitative data on prematurely aged skin so that it is not possible to quantify its relationship to solar radiation. On the other hand, there are data on skin cancer--the most common of all cancers--that indicate a close association with exposure to sunlight, particularly the uv component of sunlight.

A. EVIDENCE LINKING CANCER WITH EXPOSURE TO THE SUN

Statistics show that skin cancer is more prevalent in geographical locations near the equator than at higher latitudes. The incidence doubles with each 8-11 degree decrease in latitude. This latitude effect is significant because incident uv radiation increases from the poles to the equator. A person living in Texas receives considerably more uv-B than a person living in Minnesota, assuming that both spend the same amount of time in the sun. There are, of course, other factors that must be reckoned with in dealing with these statistics, including local cloudiness, lifestyle and hours of outdoor exposure, hereditary genetic differences, and the amount of natural pigmentation (which serves as a built-in filter). However, the incidence of skin cancer and the mortality due to skin cancer are better correlated with the intensity of uv-B radiation than with any other environmental variable.

Of the two different general types of disease that come under the broad category of skin cancer, malignant melanoma is the most dangerous; the prognosis for malignant melanoma is similar to that for breast and other commonly known cancers. The more common non-melanoma skin cancer, although rarely lethal, is disfiguring, expensive, and ultimately very limiting--if a person develops one skin cancer then he is advised to limit his exposure to sunlight in an attempt to control recurrence. Moreover, the problem of an increase in the incidence of skin cancer will not necessarily be solved by better medical care alone. Prophylaxis is unrealistic--people will simply not protect themselves by staying out of the sun. For example, although Queensland, Australia, has the highest incidence of skin cancer in the world, the population does not protect itself any more than do less susceptible populations.

Because the association of skin cancer with solar uv radiation is strong, it is reasonable and prudent to analyze the epidemiological evidence in terms of incidence (or mortality) as a function of uv flux. An extensive description of skin cancers and the epidemiological data will be found in Appendix C. The following are brief summaries of the biological evidence that leads us to associate solar uv light in the range 295-320 nm with human skin cancer in light-skinned individuals.

Basal- and squamous-cell carcinomas are the most common forms of skin cancer. Their association with exposure to sunlight may be summarized as follows:

1. They occur almost exclusively on exposed areas of the body that receive high light intensities: nose, ears, cheeks, back of the neck, etc.

2. There is higher incidence among outdoor workers: farmers, sailors.

3. There is higher incidence among fair-skinned people: Celtic, albino-Indians of Panama.

4. There is higher incidence at low latitudes (see Figure 3).

Their association with the uv-B component of sunlight may be summarized as follows:

1. Wavelengths known to be effective in producing erythema (sunburn) are below 320 nm (see Figure 4). Injury of the skin by the sun is most likely the principal stress factor in inducing skin cancer. Sunburn and skin cancer arise in the same tissue, and individuals who sunburn easily have a higher than average probability for developing skin cancer.

2. In numerous experimental studies on mice, wavelengths below 320 nm were effective in inducing skin cancer. Longer uv wavelengths were ineffective, although a recent experiment indicates that they may accentuate the effects of shorter-wavelength radiation.

3. There is good evidence that skin cancer arises from uv-induced changes in DNA--the carrier of genetic information in living cells. Wavelengths below 310 nm are hundreds of times more damaging to DNA than are the wavelengths in excess of 330 nm (see Figure 4). Ultraviolet light is mutagenic, and since many chemical carcinogens are also mutagens (i.e., affect DNA), we expect uv light to be carcinogenic by virtue of its action on DNA. Individuals with the disease xeroderma pigmentosum are extraordinarily susceptible to skin cancer induced by sunlight (in one study a prevalence of greater than 50 percent by age 10). The cells of these individuals are defective in at least one of several molecular mechanisms that repair uv damage to DNA. Hence, there is a strong implication that damage to DNA that is not properly repaired leads to cancer.

The available evidence indicates that the spectral sensitivity for skin cancer is similar to either the action spectrum for erythema production or the spectrum for damaging DNA. The two spectra are similar but not quite identical (see Figure 4).

Malignant melanoma is much rarer than the skin carcinomas mentioned above, but its mortality rate is about one third of the incidence. Its occurrence is also associated with exposure to sunlight through the following observations:

1. It occurs on exposed areas of body but not exclusively those that receive the highest intensity.

2. There is higher incidence among fair-skinned people.

3. There is higher incidence at low latitudes.

Its association with the uv-B component of sunlight can be summarized as follows:

1. Sunburn and melanoma arise in the same tissues, and individuals who sunburn easily have a higher than average probability for developing skin cancer

2. Although uv irradiation alone does not give rise to melanomas in mice, irradiation of a chemically induced benign pigmented lesion does do so.

3. Individuals with xeroderma pigmentosum (see above) have an extraordinarily high prevalence of melanoma compared with the average population. (A recent study observed a prevalence of 7 out of 15 for these individuals compared with about 2 per 10,000 for the average population.)

Although the evidence associating uv-B with malignant melanomas is not so strong as for non-melanoma, we believe that the only action spectra that we can prudently use for any quantitative estimate of the potential hazard arising from an increase in uv-B are those given in Figure 4.

B.ESTIMATION OF THE EFFECT OF INCREASED uv-B ON THE INCREASE OF SKIN CANCER AMONG LIGHT-SKINNED INDIVIDUALS

There have not been any reports of skin cancer that resulted from therapeutic uv irradiation of skin or from treatment of skin diseases with other agents that also are carcinogenic in mice. However, there have not been any long-range studies, or any comparisons between such treatments and animal experiments, that would permit quantitative estimates of skin-cancer hazards of therapeutic uv irradiation of man.

Even though there is a problem about extrapolating quantitatively from skin cancer in mice to skin cancer in man, we do know that the molecules of mice are similar to those of man and that the photochemical reactions in both mouse and human cells are similar to reactions in solution. The scientific community cannot do laboratory experiments on uv-induced skin cancer in man; and even if it could, it would take too many years for the results to be available. Hence we are forced to rely on the wealth of photobiological data that indicate that uv irradiation is harmful for the cells of all creatures and to use action spectra similar to those in Figure 4, combined with epidemiological data, to estimate reasonable values for the increase in skin cancer resulting from an increase in uv-B.

The epidemiological data used by the Panel to Review Statistics on Skin Cancer of the Committee on National Statistics of the National Research Council are summarized in Figure 3. They are described in greater detail in Appendix C. That Appendix also discusses the problems associated with using such data for quantitative prediction. Laboratory and clinical evidence suggests a causal relation between uv-B and skin cancer and therefore suggests an empirical study of the relations between observed incidence and mortality of skin cancer and the intensity of uv-B for a number of locations. Our understanding of the skin-cancer process from an epidemiological point of view is quite limited. We do not know the quantitative answers to many important questions, including which variables in addition to uv flux are important. We have good theories as to the uv wavelengths that are important for skin cancer, but we do not know how the division of total exposure into doses determines the effectiveness of a given total exposure or how the way in which we live determines both total exposure and its division into doses. Without this knowledge, the best approach seems to be to learn what we can from the available data for skin-cancer rates by place, age, and sex.

Among the simple measures of the incidence of skin cancer and of the uv flux, the ones that are mutually related in an almost linear manner are (a) the logarithm of the incidence and (b) the flux, defined as the number of photons per square meter per second per nanometer averaged over the year (see Figure 5). Moreover, use of these variables leads to residuals of about the same size for different flux levels. As a consequence, all the analyses reported here are based on linear relations involving these two variables, either alone or in combination with others (see Appendix C).

The simple relation takes the form = + ßF, where is the log incidence (or mortality), and ß are constants to be fitted, and F is a computed uv flux. The fit for 14 combinations of sexes (2) and age-groups (7) is good in the large but not completely satisfactory in detail; individual geographical areas are often consistently above or below the fit for all combinations of age and sex. Clearly there are other variables (perhaps physical or related to lifestyle; see Appendix C) that make definite, but not large, contributions to the observed log incidences. Until these variables are identified--and measured--we have little choice but to use the simple relationship above and let these additional variables contribute to our uncertainties.

Because the other relationships studied are so poorly determined with so few observations, we have chosen to present the results of analyses of log incidence (or mortality) and uv flux alone and to discuss in Appendix C the difficulties that arise when more complicated, but potentially useful, models (i.e., interpolation and extrapolation formulas) are tried out.

Table 5 gives estimates and statistically determined confidence intervals for percentage increase in skin-cancer incidence and mortality for an increase in uv-B associated with a 10 percent ozone reduction. The predictions are for two geographical locations and make use of a wavelength sensitivity intermediate between that for action on DNA and that for sunburn. Further discussion and tables with more detail appear in Appendix C. In view of the strong possibility that other environmental factors influence skin-cancer statistics, the actual uncertainties in the predicted increases in skin cancer are greater than indicated in Table 5. How much greater is far from clear. Accordingly, the confidence intervals proposed should be interpreted as minimum uncertainties. Nevertheless, although the predictions in Table 5 cover a wide range and are not completely consistent, they provide strong evidence that increases in uv will produce increases in skin cancers. The model predicts that a 10 percent decrease in stratospheric ozone will give rise to about a 20 percent increase in melanoma mortality. However, a 10 percent decrease in stratospheric ozone appears to give more than a 20 percent increase in the incidence of skin cancer--possibly a 30 percent increase.

Several other estimates of the percentage increase in skin cancer that would result from a decrease in ozone are summarized in CIAP Monograph 5, Chapter 3. These estimates employed similar carcinogenic action spectra but different models than reported above. They used many fewer data than used by the Panel on Skin Cancer Statistics. There is good qualitative agreement among the various estimates that a 1 percent decrease in stratospheric ozone would cause a 2 percent increase in skin cancer.

III. Ultraviolet Sun Exposure and Living Organisms Other Than Man

Living organisms withstand the damaging effects of uv-B by four principal means: protective coverings and pigmentation, behavioral adaptation to avoid the sunlight, photoreactivation or photoprotective mechanisms, and dark repair mechanisms. Many forms of life have developed one or more of these protective mechanisms sufficient to tolerate existing levels of uv-B radiation. A significant increase of uv-B can be expected to precipitate a disturbance in the existing balance of life.

A. EXPERIMENTAL LIMITATIONS

It is difficult to determine the effect that increases in uv-B will have on ecological balance. Wide variation in uv levels occurs over the globe naturally; the range of natural variation of uv over latitude alone far exceeds any changes that might be caused by aircraft fleets of moderate size. While species have adapted to uv, they have also adapted to climate and soils, which also vary geographically. One cannot assume that, if uv were increased globally, plants and animals that have learned to survive at high uv levels at low latitudes would then migrate to higher latitudes--to do so would require readaptation in many other ways as well.

Experiments to determine the consequences of reduced or enhanced uv-B in sunlight on living organisms are difficult to perform. Plants and animals that naturally live at high latitudes can be moved to lower latitudes and observed in uv-enhanced sunlight, but the climate must be controlled to simulate the lower temperatures, humidity, and reduced total sun exposure characteristic of higher latitudes. This approach cannot be used with plants and animals that already live in the tropics. Electric lamps can be used to supplement the uv of natural sunlight. Unfortunately, the only lamps available today also emit appreciable levels of longer-wavelength uv (e.g., a strong emission line at 365 nm), and there is evidence that presence of other wavelengths may modify the effects of uv-B. Improving lamp technology will require several years. In supplementation experiments attempting to simulate a 50 percent ozone reduction, the adverse effects of increased uv-B tended to be diminished when high intensities of visible light were also present, indicating the significant role of photorepair and photoprotective mechanisms in nature. Similar photoprotection was also observed in insects. Since reduction of ozone changes the intensities of only the shorter wavelengths, it is difficult to use simple supplementation experiments to predict quantitatively the consequences of ozone reduction. The study of the effects of uv-B on aquatic systems has been hampered by the paucity of reliable measurements on the penetration of uv-B into natural waters of the sea.

An alternate approach is to selectively delete uv-B using Mylar plastic filters or take into account the natural filtering effects of seawater for aquatic studies. Such deletion experiments indicate that present ambient levels of uv-B exert an inhibitory effect on photosynthesis in phytoplankton (sea life). Similar experiments on higher plants under field conditions indicate essentially no effect.

B. A FEW CONCLUSIONS ABOUT PLANTS AND uv-B

The conclusions outlined below are derived mainly from studies sponsored by the Department of Transportation. These studies and other relevant data are summarized in CIAP Monograph 5 (especially Chapter 3). Some of the data are given in Appendix D.

Deletion experiments are of questionable validity, because existing protective mechanisms, such as photoreactivation, may counteract the deleterious effects of uv-B. To date, experiments under field conditions have been largely of the deletion type because of the technical difficulties of large-scale supplementary irradiance--the energy requirements alone make supplementation experiments in the field almost prohibitive. However, the Panel believes that deletion experiments on plants, showing little or no detectable effect under field conditions, should not be taken to predict the consequences of increased levels of uv-B radiation.

The more useful experiments to date are those that have used supplemental uv-B radiation in growth chambers, in greenhouses, or in the field. In the studies sponsored by the Department of Transportation, supplemental uv-B was designed to simulate the effect of a 50 percent reduction of ozone. This simulation suffered from the fact that light included uv-A (at 365 nm) as well as uv-B. As a control, the light was screened with Mylar allowing only the uv-A to come through. The following results emerged from these studies:

1. Plants exposed to supplemental uv in growth chambers or in greenhouses showed 20 to 50 percent inhibition of growth. The Mylar control (uv-A only) caused less than half this degree of inhibition. Experiments in the field on the effects of supplemental uv on plant growth showed smaller, but statistically significant, decreases for some species.

2. Plants exposed to supplemental uv in growth chambers showed a 10 to 30 percent decline in chlorophyll content, accompanied by a similar decline in their capacity for photosynthesis.

3. Plants exposed to supplemental uv in the field developed degenerative changes in the structure of some of their cells. The frequency of harmful mutations, most easily scored as abnormal or missing stamen hairs, was increased sevenfold by uv-A alone (Mylar control) and twentyfold by the full supplemental uv-A plus uv-B.

4. Seedlings are more sensitive to uv than are mature plants, and single-celled algae are many times more sensitive. A few hours' exposure to natural sunlight is enough to kill many types of single-celled algae, and a 50 percent reduction of ozone is expected to decrease the lethal exposure time by more than a factor of 2.

Although the experiments on plant growth in the field were not completely conclusive, and although it is hazardous to interpolate from the 50 percent reduction level, the research sponsored by the Department of Transportation's CIAP during its short existence has laid valuable groundwork. Much more research is clearly needed before the effects of ozone reduction at levels of 10 percent or less can be predicted with confidence.

C. UV-B AND INSECTS

Some information about the effects of uv-B on insects is available. Mortality of insect larvae in cages is increased by supplemental uv, but in nature these larvae keep themselves sheltered from the sun. The eyes of insects are equipped to detect uv and to see patterns of polarized light that indicate the position of the sun. They are guided in feeding and in pollinating by uv reflectance patterns on flowers. Mate selection, at least in some butterflies, depends on visual cues that include uv reflectance patterns. A single small-scale experiment has been conducted to see what insects might do when the uv illumination on alfalfa plants in the field is increased in the uv-B range corresponding to a 50 percent reduction of ozone; this experiment gave no statistically meaningful results.

D. EFFECTS OF uv-B ON AQUATIC SYSTEMS

Primary production in the ocean depends on the photosynthetic activity of a whole range of species of living organisms. Because of the unique importance of phytoplankton and zooplankton to the ecology of the world's food chain, the sensitivity of these species to enhanced levels of uv-B is of prime concern. Elucidation of this question requires a thorough understanding of how deeply various wavelengths of uv penetrate natural waters. A few preliminary measurements of the penetration of uv-B into natural waters have been made using the Robertson uv sensor, but unfortunately this sensor is incapable of measuring the integral of radiance with a large enough solid angle to take into account diffuse radiation coming from the scattering effect of the atmosphere and of the ocean. Development of new instruments will be required for this purpose. At this time, no precise relationship between turbidity and penetration of uv-B radiation into seawater has been determined. Until this information is available, is related in some way to the vertical distribution of planktonic organisms, and is averaged meaningfully over the major population of plankton in the seas, it will not be possible to predict the effects of ambient or increased uv-B on marine plants and animals.

IV. Conclusions and Recommendations Regarding the Potential Biological Effects of Reducing Stratospheric Ozone

Laboratory experiments have shown that all unshielded cells are highly vulnerable to sunlight and may be killed by relatively short exposure to full sunlight. While such cells and organisms are generally protected to varying degrees in nature so that they experience sublethal doses of radiation, any increase in uv radiation could be considered to increase the pressure against survival. Because of the relationships between species in ecosystems, damage to one species might jeopardize an entire ecosystem. Hence, the potential effects of any elevation of the present uv-B levels of sunlight reaching the earth's surface should be taken most seriously and studied thoroughly.

There are persuasive, almost compelling, biological and medical arguments that uv-B is a cause of skin cancer. Statistical analyses show that uv radiation is associated with skin cancer, but the magnitude of the effect is indicated only within rather wide limits. The only relationship that has been found consistently to be applicable to a number of different data sets from different sites is log incidence (or mortality) linearly dependent on uv irradiance. A 10 percent decrease in stratospheric ozone causes about a 20 percent increase in melanoma mortality. However, while a 1 percent decrease in stratospheric ozone causes roughly a 2 percent increase in the incidence of skin cancer, a 10 percent decrease in stratospheric ozone appears to give more than a 20 percent increase in the incidence of skin cancer--possibly a 30 percent increase. The statistical results and predictions presented in Table 5 are preliminary and may be changed as a result of further analysis. The general pattern of the results is not likely to change, but explicit and useful relationships identifying environmental factors other than uv radiation may be found. Considerably more research is needed to establish the quantitative nature of these relationships.

The effects of uv-B on organisms other than man could also be deleterious, with some organisms being much more sensitive to this radiation than others. The Panel CONCLUDES that considerably more research is needed before the effects of increased levels of uv radiation on living organisms and natural ecosystems can be adequately predicted. Much time will be required not only to determine the direct effects of uv radiation on a particular organism but also to recognize the more subtle and long-term influences on the total ecosystem. The Panel BELIEVES that any conclusions on the effects of ozone reduction on living organisms must be of limited scope at the present time because there are potentially great deleterious effects as yet unevaluated. The time for biological studies in CIAP has been too short even to design and execute reliable short-term field-scale experiments. It is imperative that follow-on biological studies be undertaken.

We RECOMMEND that biological and medical studies of the effects of changes in ultraviolet radiation upon living organisms be increased. In particular, we RECOMMEND that studies of skin cancer be accelerated to obtain better quantitative understanding of the cause of the disease. Specific studies needed are (1) the earth-based monitoring program; initiated during CIAP should be pursued in conjunction with atmospheric monitoring and should include continuous measurements of uv-B and total sunlight at a number of stations at both high and low latitudes (greater than 55deg. and less than 10deg.) for at least five years; (2) a program is needed to gather epidemiologic data on prevalence of non-melanoma skin cancer over a wide span of latitudes and incidence data, including age of onset versus uv-B, sex, occupation, exposure habits, and skin phenotype; (3) a study should be made of the penetration of uv-B into natural waters--uv-B sensors to measure diffuse irradiance under water need to be developed; (4) a research program should be set up to study the effects of uv-B on living organisms from microbial forms to higher plants and animals--a funding commitment should be made over sufficient periods of time (up to five years) for those projects that require a prolonged period of experimentation and data collection.

This chapter presents the findings of the Panel on Biological and Medical Effects: R. Setlow, Chairman; W. Baier, W. Butler. R. Clayton, E. Deevey, T. Fitzpatrick, A. Giese, D. Gordon, F. Haxo, E. Runge, E. Scott, and F. Urbach. Consultant to the Panel: M. Caldwell.