[Emerging Infectious Diseases * Volume 3 * Number 3 * July-September 1997]

Perspectives

DDT, Global Strategies, and a Malaria Control Crisis in South America

Donald R. Roberts, Larry L. Laughlin, Paul Hsheih, and Llewellyn J. Legters

Uniformed Services University of the Health Sciences, Bethesda, Maryland,
USA
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      Malaria is reemerging in endemic-disease countries of South
      America. We examined the rate of real growth in annual parasite
      indexes (API) by adjusting APIs for all years to the annual
      blood examination rate of 1965 for each country. The
      standardized APIs calculated for Brazil, Peru, Guyana, and for
      18 other malaria-endemic countries of the Americas presented a
      consistent pattern of low rates up through the late 1970s,
      followed by geometric growth in malaria incidence in subsequent
      years. True growth in malaria incidence corresponds temporally
      with changes in global strategies for malaria control.
      Underlying the concordance of these events is a causal link
      between decreased spraying of homes with DDT and increased
      malaria; two regression models defining this link showed
      statistically significant negative relationships between APIs
      and house-spray rates. Separate analyses of data from 1993 to
      1995 showed that countries that have recently discontinued
      their spray programs are reporting large increases in malaria
      incidence. Ecuador, which has increased use of DDT since 1993,
      is the only country reporting a large reduction (61%) in
      malaria rates since 1993. DDT use for malaria control and
      application of the Global Malaria Control Strategy to the
      Americas should be subjects of urgent national and
      international debate. We discuss the recent actions to ban DDT,
      the health costs of such a ban, perspectives on DDT use in
      agriculture versus malaria control, and costs versus benefits
      of DDT and alternative insecticides.

Malaria is reemerging in most disease-endemic countries of South America
(Figure 1). Even though disease incidence is increasing, the level of
increase is undefined. More importantly, the reasons for the increase in
malaria rates after decades of successful disease control have not been
assessed. Herein we will show how rapidly malaria is increasing, examine
the patterns of resurgent malaria in relationship to the Global Malaria
Control Strategy (1), and test the hypothesis that increased malaria is due
to decreased spraying of homes with DDT. Also, we will discuss recent
actions to ban DDT, the health costs of such a ban, perspectives on DDT use
in agriculture versus malaria control, and costs versus benefits of DDT and
alternative insecticides.

Revised Estimates of Malaria Rates in South America

The Pan American Health Organization has been compiling and reporting
malaria data since 1959. These data are used to compute the annual parasite
index (API) and the annual blood examination rate (ABER). API is the number
of positive slides per 1,000 population. For each country, API can be
viewed as a measure of numbers of cases detected and numbers of cases
treated. API is based on composite data derived from both active and
passive case detection; e.g., 63% of all blood slides taken in the Americas
during 1994(superscript 1) were from passive case detection (2). [Image]

Figure 1. [Figures not available in ASCII.]
Distribution of malaria in South America (2-5). Color codes
correspond to annual parasite indexes as reported by the Pan American
Health Organization.

Figure 2.  [Figures not available in ASCII.]
Annual parasite indexes and population growth,
Brazil, 1965-1995 (2-5). A graphical representation of data
compiled by the Pan American Health Organization.

API is commonly used to compare amounts of malaria within  
geographically or temporally distinct human populations.
The formula for calculating API is

API for year x = 1,000 (number of positive slides/total population)

The number of positive slides (numerator of the API formula) for a given
year is a function of the slide positivity rate (which indicates intensity
of malaria within the environment) and the total number of slides examined.
The total number of slides examined is used to calculate ABER, which
indicates case detection effort. The formula for calculating ABER is

ABER for year x = 100 (number of slides examined/total population)

ABER represents the number of slides examined per 100 population.

The general pattern presented by conventional APIs for Brazil (2-4) is
presented in Figure 2. Our analysis shows that population growth, combined
with decreased numbers of slides examined, underestimates upward trends in
malaria cases.

Figure 3. [Figures not available in ASCII.] Slides examined and
Brazil, 1965-1995 (2-5). Points correspond to data compiled by the
Pan American Health Organization.]

The population of Brazil has grown continuously (Figure 2). The number
of blood slides examined each year increased from 1965 to 1985, and then
started an erratic decline (Figure 3). Slide positivity rates            
progressively increased after 1979 (Figure 3). Variable numbers of 
slides examined, combined with population growth, resulted in ABER
values from 2.1 to 2.55 until the mid-1980s; after 1985, ABERs steadily
declined (Figure 4).

Given the quantitative components of API, a comparison of indexes is
meaningful only if numbers of slides examined relative to the population
base are comparable across years. To illustrate, a population of 4,000,000
(with 200,000 slides examined and 60,000 malaria-positive slides) equates
to a 30% slide-positivity rate and an API of 15. However, if 400,000 slides
are examined, the API will be 30. This example shows how sensitive API is
to the number of slides examined.

We recalculated APIs for Brazil by using the slide-positivity rate for each
year and a standardized ABER of 2.31 (ABER for Brazil in 1965). The number
of slides examined for each year was recalculated as follows:

Figure 4. [Figures not available in ASCII.]
Annual blood examination rates and standardized annual
parasite indexes, Brazil, 1965-1995 (2-5). The standardized APIs were
adjusted to a common sample size across years (the annual blood
examination rate of 1965). Original data for calculating the
standardized APIs were obtained from in Pan American Health Organization
reports (2-5).

Number of slides examined/year = (2.31/100)(total population)

Using this formula for each year, we multiplied the original proportion of 
positive slides for each year by the revised estimate of total number of
slides examined. This calculation provided a uniform estimate of        
malaria-positive slides. We then divided the estimate of             
malaria-positive slides by the population of Brazil for each year 
the series. These quotients, multiplied by 1,000, produced APIs
that were standardized for sampling effort (ABER).

When the derived or standardized API is plotted (Figure 4), the pattern of
increasing quantities of malaria is very different from Figure 2. The
pattern in Figure 4 shows stable or small yearly increases in malaria rates
from 1965 to the late 1970s. After 1978, APIs increased fivefold through
1995. Similar relationships were found with years versus standardized
indexes for falciparum and vivax malarias (not shown). Standardized APIs
were also developed for Peru and Guyana (2-4). Like Brazil, Peru and Guyana
show geometric growth in numbers of malaria cases (Figure 5)(also for
falciparum and vivax malarias [not shown]).

It might be argued that the appearance of increasing malaria is an artifact
of increasing reliance on passive case detection. Such an argument is
equally valid against conventional APIs since the sources of blood smears
are the same for both the conventional and standardized indexes.

Figure 5. [Figures not available in ASCII.] Standardized annual
parasite indexes, Peru (1959-1995) and Guyana (1960-1995). The original
data were derived from Pan American Health Organization reports (2-5).
The APIs were adjusted to a common sample size across years (the annual
blood examination rate of 1965).

We concede that increased use of passive case detection contributes to
increasing slide-positivity rates; however, passive case detection is not 
sufficient to account for the magnitude or consistency of increases
described in Figures 4 and 5. Using Brazil as an example, more than 35% of
slides were taken through passive case detection in 1972.(superscript 2)
In 1991, 32.8% of all slides in Brazil were obtained through passive
case detection (5). Clearly, the 17-year pattern of increasing malaria is
not due to increased reliance on passive case detection.

The Global Malaria Control Strategy

The policies and strategies of the World Health Organization, the Pan
American Health Organization, and national donor agencies contributed to
the successful control of malaria from the late 1940s to the late 1970s
(6-8). However, the policies and strategies of these organizations have
changed (8). In 1979, the World Health Organization Expert Committee on
Malaria (9) developed a new malaria control strategy with four tactical
variants. Variants 1 and 2 included no organized vector control measures.
Variant 3 included limited vector control, and only variant 4 included, for
highly qualified countries, countrywide vector control. The goal for
variant 4 was specified as eradication, not sustained malaria control. The
new strategy was adopted by the 31st World Health Assembly as resolution
WHA 31.45 (9). During this assembly, the Director-General of World Health
Organization stressed the importance of including curative and preventive
services, including control of infectious diseases (malaria control), in
the framework of primary health care. In 1985, the 38th World Health
Assembly adopted resolution WHA 38.24, which recommended that malaria
control be developed as an integral part of the national primary health
care system (8). In October 1992, the Ministerial Conference adopted the
Global Malaria Control Strategy that had been developed at World Health
Organization interregional meetings in 1991 and 1992 (1). The Global
Malaria Control Strategy calls for deemphasis of vector control and
emphasizes case detection and treatment. The first conclusion and
recommendation of the report is that malaria control should be fully
integrated into general health services and should reflect socioeconomic
development objectives. The World Health Assembly resolutions and committee
reports document, from 1979 to the present, general, and sometimes
specific, policy decisions that promote case detection and treatment and
deemphasize residual spraying for national malaria control programs.

Failure to maintain control over malaria most likely results from failures
in the functions of interventions or from failures to make proper
application of interventions. Although DDT resistance is often posed as a
reason for malaria control failure, resistance of vector populations to DDT
is not widespread in South America (10).

There are two common interventions for reducing malaria transmission within
human populations. One potential intervention is case detection and
treatment. The second is spraying insecticide on house walls to prevent
malaria transmission inside the houses.

DDT and the Reemergence of Malaria

Field studies of DDT action against malaria vectors provide dramatic
evidence of reduced human-vector contact (11-13). However, the effect of
DDT against human malaria cannot be definitively answered by vector studies
alone. Consequently, we studied the effect of DDT on malaria rates with
regression models to look at the interactive effects of home-spray and
malaria rates across years of malaria control activities. Once missing data
were factored into the analyses, 28 and 32 years of malaria control data
were used in separate tests for Brazil and Ecuador, respectively. Brazil
was selected because it has sustained a robust malaria control program with
progressive decreases in numbers of houses sprayed with DDT (Figure 6).
Ecuador also reported progressive decreases in numbers of houses sprayed
with DDT. However, Ecuador also reported great vacillations in spray rates
(Figure 6), which were accompanied by variations in malaria rates. Data
presented in Pan American Health Organization reports (2-5) were used in
these analyses; i.e., malaria rates were not standardized by a fixed ABER.

Figure 6.  [Figures not available in ASCII.]  House-spray rates (HSRs) with
DDT, Brazil and Ecuador, 1959-1993.  Points correspond to data compiled by
the Pan American Health Organization (2-5).

Preliminary tests with a normalized API variable as the
dependent variable and house-spray rates (HSRs), time, and ABER as   
independent variables showed statistically significant negative
relationships between HSR and API values. However, the normalized   
response variables did not fulfill the requirement of constant
variance, and the model exhibited problems of autocorrelation.

The problems with data variance and autocorrelation were solved for Brazil
data by performing analyses with the following regression model:

gamma (subscript t) = alpha + beta (subscript 1) gamma (subscript t-1) +
beta (subscript 2) chi (subscript -1) + epsilon

The gamma represents an API value and t is time (year). Given that
gamma (subscript t) represents API for year t, then gamma (subscript t-1)
represents API for the preceding year. This component
of the formula represents a lag year API value. The alphais intercept,
and beta is a parameter (slope) of the gamma regression line.
The HSR is from the year preceding gamma (subscript t),
represented by chi (subscript t-1). Last, beta (subscript 2)
is slope of the HSR regression line, and epsilon is the residual
effect not accounted for by the API and HSR
variables. This formula captures the idea that API plus HSR of one year can
be used to accurately predict the API of the following year.

The analysis of variance of 28 years of data from Brazil produced an
excellent fit of the regression model (F = 354; df=(2,26); p < 0.0001). The
adjusted r (superscript 2) for the regression analysis was 0.96. Parameter
estimate for  gamma (subscript t-1) was 0.74, and this relationship was highly
significant (p < 0.0001). The parameter estimate for chi (subscript t-1)
was -0.0174; it was also highly significant (p < 0.0004).
A test for autocorrelation was performed by correlation analysis
of residuals versus lag time residuals. The Pearson
Correlation Coefficient test statistic was used to test the null hypothesis
that rho = O. The p value was 0.87 (not statistically significant), so
we accepted the null hypothesis of no autocorrelation.

The problems of variance and autocorrelation were solved for data from
Ecuador by performing regression analyses with the following model:

gamma (subscript t) = alpha + beta (subscript 1) gamma (subscript t-1) +
beta (subscript 2) (log(chi ((subscript t-1)))
 + epsilon

The only difference between the Brazil and Ecuador models was a log
transformation of the lag HSR values. A log transformation of lag HSR
values reduced variation in this variable and produced a better fit of the
whole model.

The regression analysis of 32 years of data from Ecuador produced an
excellent fit of the regression model (F = 45.6; df=(2,30); p < 0.0001).
The adjusted r(superscript 2) for the regression analysis was 0.73.
Parameter estimate for gamma (subscript t-1) was 0.58, and this
relationship was highly significant (p < 0.0001). The parameter estimate
for log (chi (subscript t-1)) was -1.197; it was also
highly significant (p < 0.0001). The test for autocorrelation produced a p
value of 0.51 (not statistically significant), and again we accepted the
null hypothesis of no autocorrelation.

These highly predictive models showed the powerful relationship between
DDT-sprayed houses and mala
ria rates. We documented that a high API in
combination with a high HSR is predictive of a lower API the following
year. Alternatively, when low APIs are combined with low HSRs, malaria
rates are higher the following year. Therefore, when large numbers of
houses are sprayed with DDT, malaria rates decline and when fewer houses
are sprayed, malaria rates increase.

Eliminating DDT for Malaria Control

Countries are banning or reducing the use of DDT because of continuous
international and national pressures against DDT (e.g., the International
Pesticide Action Network is "...working to stop the production, sale, and
use..." of DDT [14]) and aggressive marketing tactics of producers of more
expensive alternative insecticides. It has become easier for political
pressures to succeed given the global strategy to deemphasize use of the
house-spray approach to malaria control. A recent agreement of the North
American Commission on Environmental Cooperation for eliminating the
production and use of DDT in Mexico within the next 10 years (superscript 3)
is the latest development in the campaign to eliminate DDT.

The Health Costs of Abandoning DDT

Figure 7. [Figures not available in ASCII].
Increases in annual parasite indexes for four categories of
countries, South America, 1993-1995. For each country, the populations at
moderate to high risk for malaria were adjusted to midyear (1994) values.
Data were derived from reports of the Pan American Health Organization
(2-5).

There is a cost in abandoning DDT for malaria control. This cost is seen in
the results of malaria control programs from 1993 to 1995. We can get a
uniform picture of events from 1993 to 1995 by standardizing malaria rates
according to size of population at risk for malaria in each country (3,4).
Since there were variations in this population variable for the 3 years, we
took the population estimates for the midyear interval, 1994, as the basis
for adjusting malaria rates for 1993 and 1995 (2). Each country was also
characterized according to its reported use of DDT for malaria control in
1993 through 1995 (2-4).

As shown in Figure 7, countries that discontinued their house-spray
programs reported large increases in malaria rates. Countries that reported
low or reduced HSRs also reported increased malaria. Only Ecuador reported
increased use of DDT and greatly reduced malaria rates.

The Use of DDT in Agriculture versus Malaria Control

In 1993, North, Central, and South American countries used 1,172,077 kg of
DDT to spray house walls (4). While this may seem to be a large amount of
insecticide, it actually represents less than 6% of the DDT used in the
United States alone in 1968 (15). More than 795 kg of DDT might be used to
treat a mere 0.4 km(superscript 2) (100 acres) of cotton during a growing
season.(superscript 4) This amount of DDT would be sufficient to treat more
than 1,692 houses. At four to five persons per house, spraying 1,692 houses
translates into protection for as many as 8,460 persons.
Since rural households are the primary candidates for house spraying,
the 1,692 houses would be spread over a very large area. If a
household of five persons is used, for example, significant levels of
malaria control could be obtained for all populations
at moderate to high risk for malaria transmission in Guyana by spraying
only 17,000 houses during a single spray cycle. This level of treatment for
the whole country of Guyana, covering an area of 215,000 km(superscript 2),
is roughly equal to the amount of DDT that might be used to spray only
4 km(superscript 2) (1,000 acres) of cotton during a
single growing season. These statistics demonstrate the
differences between DDT for agriculture and DDT for malaria
control. On a landscape scale, a sprayed house represents an
infinitesimally small spot treatment of a closed and protected environment
(the house). DDT is relatively insoluble in water, so even when a house
collapses and decays, DDT will not easily move from the house site.

Cost versus Benefit

Based on statistics compiled in 1978,(superscript 5)costs of chemicals for
protecting a person showed malathion to be five times more expensive than DDT.
In evaluating the cost of case treatment versus insecticide spraying, it is
important to weigh the fact that a treated person will probably return to
sleep in the very house where a potentially infectious blood meal was
served to malaria vector mosquitoes the night(s) before diagnosis and
treatment. Even with treatment and cure, persons can become reinfected by
mosquitoes that fed on them before treatment. Indeed, a person can be
reinfected and undergo curative treatment repeatedly over a period of a few
months. While DDT residues do not provide complete protection from malaria
transmission, they do provide variable but significant levels of protection
for months after walls are sprayed.

A study of DDT alternatives for malaria control in Ecuador showed that the
cost of other insecticides was many times higher than the cost of $1.44 to
spray one house per year with DDT (16). The prohibitive cost of DDT
alternatives has been a problem in malaria control (16). From 1986 to 1988,
Mexico evaluated DDT alternatives in its national malaria program but
discontinued their use because of unfavorable responses and high costs
(17). High costs and downward trends in foreign aid suggest that many
countries cannot afford the switch to DDT alternatives.

In 1994, the U.S. Agency for International Development allocated only
$850,000 for malaria control in the Americas, compared with $4.13 million
for malaria vaccine research (2). National malaria control budgets in the
Americas declined 27% from 1994 to 1995, and loans and grants declined by
29%. With economic downsizing and reduced levels of foreign aid from
industrialized countries (3), there is little likelihood that more money
will be allocated for more expensive insecticides.

Discussion and Conclusions

Malaria is reemerging in disease-endemic countries. We have shown
the patterns of real growth in malaria rates for Brazil, Peru, and  
Guyana. Figure 8 shows a similar pattern of growth in malaria rates for
18 other countries of the Americas.  Figure 8 also depicts the             
relationships of increased malaria incidence to changing global          
strategies for malaria control. There is no inference of causation between  
changing policies and malaria increases. In fact, the HSRs were     
declining (as illustrated in Figure 8) even before global strategies were    
changed. However, it certainly seems that the new strategies are not      
producing a desirable outcome.       
                                     
We have used two regression models to show that as numbers of DDT-sprayed  
houses declined, malaria incidenceincreased. The period from 1959 to   
1978 can be characterized as a period of insecticide-controlled malaria. The
period from 1979 to 1995 can be characterized as a period of decreased
use of residual spraying and geometric growth in malaria incidence. Other
factors contribute to resurgent malaria, but none would appear to equal the
influence of decreases in the house-spray programs.

Figure 8. [Figures not available in ASCII.] Standardized annual
parasite indexes for 21 countries of the Americas, 1959-1995. Major
changes in global malaria control strategies are depicted with arrows
along the x axis (WHA 31.45 for 1979; WHA 38.24 for 1985; and the
Global Malaria Control Strategy for 1992). Statistical data were
derived from reports of the Pan American Health Organization (2-4).
Block A represents a period of malaria control by spraying
adequate numbers of houses with insecticide residues (primarily
DDT). Block B represents a period of increasing malaria as the
house-spray rates declined below effective levels. Open circles
represent house-spray rates and solid squares represent
standardized annual parasite indexes.

Public health researchers in the United States helped initiate the use of
DDT for malaria control in 1943 (19). Today, DDT is still needed for
malaria control. If the pressure to abandon this effective insecticide
continues, unchanged or declining health budgets, combined with
increasingly expensive insecticides and rising operational costs, will
result in millions of additional malaria cases worldwide.

DDT should be produced and distributed for governments to use in malaria
control only. Use of this insecticide should not be abandoned unless its
known detrimental health effects are greater than the effects of
uncontrolled malaria on human health.

The multifaceted issues of DDT use for malaria control (e.g., ecologic
damage, human carcinogenicity, and pesticide resistance) and the
applicability of the Global Malaria Control Strategy to the Americas should
be the subject of intensive national and international debate. We are now
facing the unprecedented event of eliminating, without meaningful debate,
the most cost-effective chemical we have for the prevention of malaria. The
health of hundreds of millions of persons in malaria-endemic countries
should be given greater consideration before proceeding further with the
present course of action.

About the Author

Dr. Roberts is professor, Department of Preventive Medicine/Biometrics,
Uniformed Services University of the Health Sciences (USUHS), Bethesda, MD.
His research focuses on modeling of malaria control methods and on the
applications of remote sensing and geographic information systems to
malaria control in the Americas.

Address for correspondence: Donald R. Roberts, DPMB, USUHS, 4301 Jones
Bridge Rd., Bethesda, MD 20814; fax: 301-295-3860; e-mail:
droberts@usuhsb.usuhs.mil.

References

  1. World Health Organization. Implementation of the global malaria
     control strategy. World Health Organ Tech Rep Ser 1993; no. 839.
  2. Pan American Health Organization. Status of malaria programs in the
     Americas. XLIII Report. Washington (DC): PAHO; 1995.
  3. Pan American Health Organization. Status of malaria programs in the
     Americas. XLIV Report. Washington (DC): PAHO; 1996.
  4. Pan American Health Organization. Status of malaria programs in the
     Americas. XLII Report. Washington (DC): PAHO; 1994.
  5. Pan American Health Organization. Status of malaria programs in the
     Americas. XL Report. Washington (DC): PAHO; 1991.
  6. World Health Organization. Sixth Report, Expert Committee on Malaria.
     World Health Organ Tech Rep Ser 1957; No. 123.
  7. Brown AWA, Haworth J, Zahar AR. Malaria eradication and control from a
     global standpoint. J Med Entomol 1976;13:1.
  8. Gilles HM, Warrell DA. Bruce-Chwatt's essential malariology. Boston:
     Edward Arnold; 1993.
  9. World Health Organization. Seventeenth Report, WHO Expert Committee on
     Malaria. World Health Organ Tech Rep Ser 1979; No. 640.
 10. World Health Organization. Resistance of vectors of disease to
     insecticides. World Health Organ Tech Rep Ser 1980; No. 655.
 11. Roberts DR, Andre RG. Insecticide resistance issues in vector-borne
     disease control. Am J Trop Med Hyg 1994;50:21.
 12. Roberts DR, Alecrim WD. Behavioral response of Anopheles darlingi to
     DDT-sprayed house walls in Amazonia. Bull Pan Am Health Organ
     1991;25:210-7.
 13. Rozendaal JA. Behavioral responses of Anopheles darlingi in Suriname
     to DDT residues on housewalls. J Am Mosq Control Assoc 1989;5:351-8.
 14. Pan American Health Organization. PAHO Environmental Series
     1993;12:53.
 15. Agricultural Stabilization and Conservation Service. Pesticide review.
     United States Department of Agriculture; 1968.
 16. Arellano F. Uso de insecticidas en el programa de control de la
     malaria del Ecuador. Estrategia aconsejada. In: Comit Rotario
     Interdistrital Andino de Lucha Contra la Malaria, editors. Nuevas
     estrategias contra la malaria. Quito, Ecuador: Rotario Interdistrital
     Andino de Lucha Contra la Malaria; 1990.
 17. Bruce-Chwatt LJ. The cost of malaria and of its control in relation to
     socio-economic realities. In: Study Group on Malaria in the Americas,
     editors. Washington (DC): Pan American Health Organization, 1977.
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     pblica Estados Unidos Mexicanos, 1957-1987. In Proceedings of "Taller
     sobre resistance," PAHO meeting 1988 18-29 Julio, Guatemala.
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(superscript 1) This percentage was obtained by adding the number of slides from passive
case detection reports and from voluntary collaborators and then dividing
the sum by the number of slides acquired through active case detection.

(superscript 2) Statistics drawn from a U.S. Agency for International Development review
in 1973-1974 of the malaria eradication program in Brazil and based on
regions that were in the attack phase. There was greater reliance on active
and epidemiologic surveys in such areas than in areas of consolidation or
maintenance. Therefore, the overall percentage of slides derived from
passive case detection was undoubtedly higher than 35%.

(superscript 3) The Commission for Environmental Cooperation (CEC) is a North American
environment commission established by a North American Free Trade Agreement
side agreement. The CEC draft agreement entitled "North American Regional
Action Plan on DDT, Task Force on DDT and Chlordane," dated October 10,
1996, calls for the elimination, distribution, and use of DDT for malaria
control in Mexico in 10 years.

(superscript 4) Recommended weekly treatments of 0.9-1.36 kg (2-3 pounds) of DDT per
0.004 km(superscript 2) (1 acre) of cotton. Using a 7-week period and a treatment
of 1.13 kg (2.5 pounds) per 0.004 km(superscript 2), 340 kg (1.750 pounds)
of DDT is required for 0.4 km(superscript 2) (100 acres) of cotton.

(superscript 5) World Health Assembly document A31/19, 1978.

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Emerging Infectious Diseases
National Center for Infectious Diseases
Centers for Disease Control and Prevention
Atlanta, GA

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