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IV. Managing Conditions during Plant Growth and Ear Development

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Environmental stTesses on plants, diseases, and insects


Wind, water, and insect borne spores from colonized debris, sclerotia, and soil sources



Whorl to silking

L -Infection



and Colonization period-




t H a r v e s t period 4 4 - S t o r a g e and -b




b F t susceptible

65 time of infection 85


Approximate no. of

days post-planting




damage to grain by insects


Increasing post-infection aflatoxin accumulation


figure 1 The chronology of corn kernel infection by Aspergi/lusJ?avrts and subsequent atlatoxin contamination. Source: Widstrom ( 1992).



standard recommendation for corn grown in the South and other warmtemperature locations, especially those that have sandy soil with low waterholding capacity (N. C. Aflatoxin Committee, 1977; Glover and Krenzer, 1980,

Smith, 1981). The risk for aflatoxin contamination of corn, however, seems

always greatest under drought conditions, regardless of soil type (Tuite et af.,

1984), and the recommendation made to avoid contamination is to alleviate stress

by irrigation during the reproductive period (Jones, 1983) or adjust the planting

date to move the critical period of grain filling to a period of minimum stress

(Widstrom ef al., 1990).

All irrigated corn production systems require some form of soil moisture

monitoring to determine when irrigation is needed (Lee, 1994). Providing water

to the crop in efficient amounts at the optimum time will often determine the

profit margin for production; therefore, good judgment and experience are required for wise decisions regarding the best time to irrigate. Most growers,

experienced or not, will rely on mechanical or electronic devices to determine

when such soil moisture levels are critically low and irrigation is needed. Tensiometers or similar devices give the most reliable soil moisture measurements

and can provide moisture availability at several soil depths, giving the grower

adequate information to make a good decision on when to irrigate. This information, along with up-to-date weather forecasts, will maximize water use efficienCY.

The soil water tension in centibars required to call for irrigation will vary with

plant stage, soil type, and the adequacy of the irrigation system (Lee, 1994).

Young plants can survive slightly lower levels of moisture in the soil before

irrigation is applied, while large amounts of water are needed at the critical

flowering and grain-filling stages. Water demands are so high during the critical

stages that some plant stress is seldom avoided, especially if temperatures are

high and rainfall is limited during these periods.

In general, irrigation is called for when 20- to 25-cm-depth tensiometer readings are at 20 centibars or greater. Sandy loam soils usually require 25-40 mm of

irrigation when the critical soil moisture tension is reached. Heavier soils can

handle slightly more and sandy soils slightly less because of a lower waterholding capacity for sandy soils. Moisture deficit is among the easiest plant

stress-inducing factors to adjust and probably the most important because it

significantly impacts other stresses, such as insect damage and disease expression. Sandy soils, subject to frequent moisture deficit, along with high night

temperatures and greater disease and insect pressure, are the principal reasons

why aflatoxin contamination of corn is chronic in the southern and southeastern

United States.

Numerous studies have investigated the influence of irrigation on aflatoxin

contamination (Fortnum and Manwiller, 1985; Payne er af., 1986; Jones, 1987;

McMillian et af., 1991; Smith and Riley, 1992). These studies, without excep-



tion, demonstrated a net beneficial effect when irrigation was available. The

benefit of irrigation cannot always be realized, however, because it is often not

practical for the grower. In fact, corn is most often produced without irrigation in

high-risk areas, since more than one-half of the corn acreage in the Southeast is

grown under nonirrigated conditions. Alternative control measures must therefore be made available to growers for whom irrigation is either impractical or


2. Fertilization and Plant Nutrition

Initial observations of an increased incidence of aflatoxin contamination in

preharvest corn grown under low fertility conditions were made by Anderson et

al. (1975). This study in Georgia and others have led to a general consensus that

nitrogen fertilization of corn will influence aflatoxin contamination of the crop

(McMillian et al., 1991), even as it influences most other plant traits. The sandy

coastal plain soils of the southeastern United States are naturally very low in the

highly soluble nitrogen that is critically needed for corn, a heavy user of this

element (Gurley, 1965). Since a recommendation of adequate fertility is critical

for obtaining good yields, no serious changes in the fertilization recommended

for corn production were necessary with regard to aflatoxin contamination (Georgia Extension Aflatoxin Committee, 1978). A word of caution resulted from

experiments by Wilson et al. (1989a) when they demonstrated that overfertilization with nitrogen can also increase the incidence of contamination. This effect

can again probably be attributed to increased stresses on the plant and is a

concern only for those who are attempting to obtain maximum yields by applying

high levels of nitrogen fertilizer.

Other fertilization studies have given similar results regarding the need for a

supply of adequate nitrogen for the corn plant (Glover and Krenzer, 1980). No

single experiment can be cited as conclusive proof of the influence of nitrogen on

Contamination, since many studies also include the testing of other confounding

factors (Jones, 1983; Jones and Duncan, 1981). Stresses induced by inadequate

nitrogen for good plant growth are clearly a significant contributor to the contamination process (Payne et al., 1989). Lillehoj (1983) reasoned that since stress is

so convincingly implicated, and inadequate fertilization does induce stress, we

must include fertilization in the aflatoxin contamination equation.

The nutritional status of the plant, other than that expressed by obvious deficiency symptoms and lack of vigor, has not been demonstrated to be closely

associated with contamination by aflatoxin. Most nutritional factors have a high

impact potential on yield and are normally addressed because of their close

relationship to capacity for production. Many nutritional problems occur because

of nutrient solubility that is related to pH of the soil solution. Adjustments in pH

are made by the application of lime, as previously described.

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a. Deficiency Symptoms

Nutritional deficiencies can usually be avoided if the appropriate fertilizers are

applied in a timely manner based on soil tests. Weather or unusual edaphic

conditions may induce deficiency symptoms in the corn plant due to lack or

unavailability of essential nutrients. Unlike the symptoms of disease development and insect activity, symptoms of nutritional deficiency can often be remedied and the plant restored to a healthy condition, if soil pH is in an acceptable

range for corn growth and weather is not extreme.

Frequent field inspections (as often as twice weekly) will assist greatly in

identifying plant stress due to nutritional inadequacies. Books and pamphlets are

available which not only describe deficiency symptoms, but also give excellent

pictorial examples to assist in diagnosis (Aldrich et al., 1975). County agents are

familiar with these aids and are available to assist the grower with both the

diagnosis and the remedy. Prompt attention to deficiencies will increase production and avoid the plant stress which can predispose kernels to A. flavus infection

and aflatoxin contamination.

b. Tissue Sampling

The plant is already suffering from stress if one waits until deficiency symptoms appear. Whole plant or leaf analyses can be useful for anticipating nutritional problems if a systematic program of testing is used (Lee, 1994). This procedure is very useful after the whorl stage for systems where fertilizer can be

applied through the irrigation system. A standard range of acceptable values has

been established for the major elements and most minor elements at the various

stages of plant growth (Smith, 1990). When samples are taken on a regular

schedule, the nutritional needs of the plant can be accurately anticipated prior to

stress due to nutrient deficiency. Stresses on the plant, especially during the

critical grain-filling stage, are known to increase the risk of aflatoxin contamination, and a regimented system of tissue sampling can eliminate nutritional

stresses during that critical period.

3. Cultivation and Weed Control

Cultivation and weed control are sometimes thought of as being synonymous,

but for purposes of this discussion, cultivation includes all types of tillage and/or

disturbance of the soil. It seems that cultivation practices associated with any

crop tend to increase the incidence of Aspergillus spp. propagules in the soil.

When compared to virgin, undisturbed prairie soils which produced 0 propagules, soils under conventional tillage and a legume-grass rotation yielded 256

propaguleslgram of soil (Angle, 1987). The degradation of aflatoxin also varied

from one soil to another, in that a fertile silt loam soil was more efficient than a

silty clay loam soil at decomposing aflatoxin B , .



Cultivation practices used under different rotation systems have not been

shown to influence aflatoxin contamination of the corn crop (Smith, 1981), nor

have the practices of conventional till versus no-till. Presumably, all tillage

systems provide an adequate supply of inoculum for infection and aflatoxin

contamination when environmental conditions are favorable. One tillage practice

that has proven effective in reducing contamination is that of subsoiling. Subsoiling allows deeper root penetration and renders the plant less susceptible to stress

under drought conditions. The apparent benefit of subsoiling is accomplished by

buffering the plant against water stress (Payne el al., 1986). Subsoiling is apparently the only tillage practice proven beneficial in reducing aflatoxin contamination, although recommendations usually only refer to tillage as an influencing

factor (Jones, 1987).

A good program of weed control is a necessity for every successful corn

growing operation. Eliminating weeds will obviously reduce water usage and

assist in preventing water stress on the crop, reducing yield losses for dryland

corn. As a secondary effect, good weed control will also reduce contamination

by aflatoxin, and consequently recommendations for control of aflatoxin usually

include judicious control of weeds by chemical or other means (N. C. Aflatoxin

Committee, 1977; Glover and Krenzer, 1980). The importance of addressing

weed competition with the crop in an aflatoxin control program has not been

documented by any formal studies to this author's knowledge, but weed control

is still an obvious and necessary recommendation (Lillehoj, 1983). An investigation that compared three cultivation rates to control weeds found no significant

differences among the treatments for aflatoxin production in the preharvest crop

(Bilgrami et a / . , 1992). The extensiveness of' a weed infestation needed to

demonstrate an effect on contamination is, therefore, an academic question that

requires no answer in the practical arena.

4. Disease and Insect Involvement

Plant disease is normally manifested by unique symptoms and as a reduction in

plant vigor. As such, stress on the plant is increased and susceptibility to other

organisms is increased, including infection by Aspergillus spp. Numerous diseases are prevalent on corn, all of which have a significant impact on plant vigor,

stress, and susceptibility to invasion by fungi such as the Aspergilli. The most

critical of these diseases with respect to aflatoxin contamination would be those

affecting the ear, especially the ear rots. Although known to be a member of the

complex of fungi invading the corn ear, A . f l a w s was not considered to be a

seriously damaging ear-rot organism, probably because of its generally nonaggressive nature (Taubenhaus, 1920). Ear rots caused by other organisms such as

Helminthosporium have been long associated with the presence of Aspergillus

spp. and sometimes with aflatoxin contamination (Doupnik, 1972). Aspergillus

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,flavus is often referred to as an ear-rot organism (Campbell et al., 1993), although now recognized as well for its more notorious reputation as an aflatoxin

producer (Campbell and White, 1994). Its presence in the ear-rot complex keeps

it available for vigorous activity when conditions favor its development over

other organisms. Competition among ear-invading organisms will be discussed

in a later section of this chapter. The control of ear rots, stalk rots, and leaf

diseases has been accomplished primarily through plant breeding since chemical

control is not practical, except when growing specialty corns, sweet corn, or

breeding nurseries. Applications of several different fungicides in an experimental situation have been ineffective in significantly reducing aflatoxin contamination (Lillehoj et al., 1984; Duncan et af., 1994). The breeding approach will

undoubtedly be necessary in ultimately dealing with the aflatoxin problem.

The Aspergilli have long been associated with insect invasion of the corn ear in

addition to being members of the fungal ear-rotting complex (Taubenhaus, 1920;

Koehler, 1942). The present-day focus on an insect involvement was begun when

Anderson et al. (1975) reported preharvest contamination by aflatoxin and its

association with insect damage. Sampling studies of harvested and stored corn

conducted by the ARS at Peoria, Illinois, also began to show an association of A.

j a v u s with insect-damaged corn (Fennel1 er al., 1975, 1977). The association of

A. j a v u s and insects was examined in several preharvest field studies (Widstrom

et al., 1975; LaPrade and Manwiller, 1977; McMillian et al., 1978; Lillehoj et

al., 1978a; Zuber and Lillehoj, 1979) and subsequently the relationships between

insects, their damage to ears, and aflatoxin contamination of the corn was clearly

demonstrated (Lillehoj et al., 1975b, 1978a).

The role of insects in the infection and contamination process has been reviewed extensively (Widstrom, 1979; McMillian, 1983, 1987; Barry 1987). In

general, it has been determined that insect damage to the ear is consistently

associated with increased sporulations of A . flavus on the ear and increased

aflatoxin contamination of the grain (McMillian et ul., 1985b). This concept

holds even though other factors may tend to interfere, such as frequent heavy

dews that may cause insect damage to increase (McMillian et al., 1985a) and the

presence of A. parasiticus that is more closely associated than A . flavus with soil

insects (Lillehoj et al., 1980d).

Several investigations were initiated to determine which insects were most

closely linked to the infection and aflatoxin-producing process (Widstrom et al.,

1975). They determined that when confined to ear-feeding, the European corn

borer contributed more to the contamination process than either corn earworm or

fall arniyworm. The corn earworm is the most frequent lepidopterous ear feeder

in the South, and McMillian et al. (1990) found in a 12-year study that A . juvus

contamination of the corn earworm moth may also be closely enough associated

with preharvest contamination to serve as an early warning system to predict

eventual grain contamination by aflatoxin. A series of studies by Guthrie et al.



(1981, 1982) and McMillian et al. (1988) established the European corn borer as

a viable contributor to contamination when it occurred as an ear feeder, and only

its leaf-feeding habits prevent it from being the dominant insect associated with


The maize weevil (Sirophilus zeamais Motschulsky) is of special interest with

respect to the aflatoxin contamination problem because it functions as both a

preharvest and storage insect. Initial reports suggested that it was of relatively

limited importance and was judged to be a very inefficient vector of A . fravus

(LaPrade and Manwiller, 1977). Subsequent studies by McMillian et al. (1980a)

demonstrated that the maize weevil can contribute significantly to increased A.

jluvus infection on corn ears by transporting spores and damaging kernels. Other

investigators later confirmed the maize weevil as being an effective vector of

spores and capable of increasing aflatoxin concentration in kernels by as much as

100 times in the presence of the fungus (Rodriguez er al., 1983; Barry et a l . ,

1985). Heat and moisture generated by weevil activity in stored corn can be the

primary support for A . flavus growth (Dix and All, 1987). A recent addition to

the list of vectors is sap beetles (Nitidulidae) that can become carriers of the

fungus when both are present in the ear (Lussenhop and Wicklow, 1990). Other

ear feeders may also be capable of vectoring the fungus, but are considered

unimportant because their frequency as ear invaders is very low.

a. Prophylactic Measures

There are precautions that can be taken before planting to protect the crop from

damage and stress that will occur if insects, diseases, other pests and weeds are

not controlled. Such measures are in addition to the buiit-in precautions taken by

seed companies that provide protection through seed treatment and inherent

resistance of their hybrids to some pests and diseases. The use of prophylactic

measures often hinges on the growers’ experience with producing aflatoxin-free

corn on the farm, and more specifically in a given field. Cropping history, soil

type, availability of irrigation, and experience with site-specific production problems will be determining factors (Smith, 1990).

Band application of a nematicide, insecticide, or both at planting is an effective way to protect young plants from early stress and provide a healthy start.

This practice is especially important if nematodes or cutworm problems are a part

of the field history. Additionally, these treatments are very important for minimum tillage where opportunity for carry-over of problems from the previous

year’s crop debris is possible. Many growers also apply pop-up fertilizer at

planting to give the corn plant a fast start and improve vigor of the young


Early control of specific weeds can be achieved by choosing species or weedclass-specific herbicides, preplant incorporated into the top 5-10 cm of soil.

Weed problems are dependent on the crop rotation being practiced, weed species



distribution in the field, effectiveness of the chosen herbicide in controlling weed

species that are present, and grower tillage practices. Weed control is a routine

recommendation to aid in reducing infection by A . Javus (N. C. Aflatoxin

Committee, 1977). In general, weed problems need to be extensive for sufficient

stress on the plant to predispose it to contamination by aflatoxin during kernel

development (Glover and Krenzer, 1980; Bilgrami et al., 1992). Other sporadic

problems can severely affect the level of stress on the young corn plant, such as

thrips and nutrient deficiencies due to heavy rains that leach nutrients from the

soil. These uncertain occurrences do not warrant prophylactic measures because

of economic restrictions.

b. Control during the Growing Season

It has been a commonly held belief that contamination of the corn crop by

aflatoxin is inevitably beyond the control of the producer when conditions conducive to its formation are present. We now know that the risk of A . flavus infection

and aflatoxin contamination can be reduced substantially through a good production management system. Events which place young corn plants under stress can

have a lasting influence on their susceptibility to attack later in the season.

Management toward a healthy crop must begin early. Some stress-inducing

events have no remedy and it is already too late for corrective action when they

occur (Aldrich et al., 1975). Natural events such as flood or hail are typical

examples. Some problems can be diagnosed and corrective action can be taken.

Those for which remedial action may be effective require close scrutiny of the

crop and immediate action. Insects which attack the very young plant and destroy

it completely obviously do not contribute to the aflatoxin problem. Other insects,

such as thrips, attack in cool, dry weather and stunt growth of the young plant.

An application of irrigation water can often break the infestation cycle and allow

plants to recover fully.

The most critical time for the growing plant, from the standpoint of aflatoxin

contamination, is the grain-filling period (Fig. 1). Any insect attack that produces

stress in the plant will increase the risk of Contamination. The best defense

against insects in field corn is host plant resistance, a prophylactic tool that is

seldom supplemented by insecticides. Insecticides can be effective against leaffeeders and cell-sap feeders, but this method is not often used because of the

cost/benefit factor. The greatest impact is made by ear-feeders that feed on

kernels and expose damaged tissue for invasion by even the least aggressive

fungi, such as the Aspergilli. The concurrence of insect damage and fungal

infection of the ear has been recognized for many years (Taubenhaus, 1920). The

concurrence concept was extended to harvested corn (Fennel1 et af.,1975; Shotwell er a l . , 1977) and later to preharvest corn (Anderson et al., 1976; Wilson et

al., 1981a; McMillian et al., 1985b). Even when fields are checked twice weekly

as recommended by extension agronomists (Smith, 1990) there is often little that



can be done to eliminate the infestation after it is established inside the ear.

Reducing plant stress by irrigation and timely harvest are other measures that

help to minimize aflatoxin contamination.

Diseases, like insects, impose stresses on the growing corn plant that render it

susceptible to attack by a variety of pests and maladies, including infection by

Aspergillus and subsequent aflatoxin contamination. Most disease problems

which plague the corn plant after emergence are not easily remedied. Prophylactic measures may be the most effective in controlling disease, especially the use

of hybrids that are tolerant or resistant.

Those diseases that infect the ear are the most serious contributors to the

aflatoxin contamination problem. A complex of ear pathogens and ear-feeding

insects all interact (Taubenhaus, 1920) to make effective control difficult. Specific organisms such as Helmitithosporium maydis have been associated as predisposing agents with aflatoxin contamination of the ear (Doupnik, 1972). Certain investigators have chosen to deal with the Aspergilli as ear-rot organisms and

evaluate them accordingly (Campbell et al., 1993; Campbell and White, 1994).

The Aspergilli are now classified as causative organisms for both ear rots and

storage rots by authorities (Shurtleff, 1980), but they were considered by mycologists to be weak or nonaggressive pathogens for many years (Payne, 1987).

When diseases do appear, they often occur in localized areas within fields, or

only in certain fields (Smith, 1990).Optimum practices in irrigation and fertilization to assure a nonstressed, healthy growing plant can help to minimize the

spread of existing diseases and may even limit opportunities for others to get an

infection foothold. In essence, management to optimize production is also management to minimize the risk of aflatoxin contamination. Usually by the time

disease symptoms are expressed, it is already too late to reverse the process, and

emphasis should rather be placed on containment or limiting spread and severity.

Any evidence of mold in the ears, found during regular inspections after denting

has begun, should initiate grain sampling and testing for the presence of aflatoxin

(Smith, 1990).

Leaf-feeding by lepidopterous insects during all pretassel stages can impose

considerable stress on the plant if damage is extensive. If the infestation is

discovered early and is very heavy, an application of insecticide can be effective

and economical when one considers potential losses. Decisions regarding insecticide applications on a growing corn crop are very difficult and must be carefully

weighed to determine cost benefit, but they must be made quickly, before extensive damage, to be effective. Spot treatment may be effective if infestations are

detected early (Aldrich et al., 1975).

Experiments designed to determine if aflatoxin contamination could be eliminated if insects were removed from the picture by insecticides were conducted by

Lillehoj et a/. ( 1976~)and Widstrom el al. (1976). In both experiments the

insecticide treatments did not completely eliminate insect damage nor did they

2 46


preclude A. flavus infection or aflatoxin contamination. Studies by Draughon et

a!. (1983) indicated that certain insecticides were capable of inhibiting aflatoxin

production by A. parasiticus in the laboratory, and to some extent in the field, but

not sufficiently to assure safe use of corn that had been exposed to adequate

inoculum. The application of insecticides to control A. flauus infection would

certainly not be cost effective unless they could be relied upon to eliminate

aflatoxin contamination. Recent studies have confirmed the inadequacy of insecticides as a means to eliminate contamination (Smith and Riley, 1992).

Insects such as Heliothis virescens, an insect closely related to some of the earfeeders in corn, are susceptible to aflatoxin (Gudauskas et al., 1967). Aflatoxin

also is toxic to several other insects (Matsumura and Knight, 1967), suggesting

that A. fluvus or its toxins may function as natural control agents for some insects

(Roberts and Yendol, 197 1). McMillian ef al. (1980~)examined this possibility

for three of corn’s ear feeders and found that dosages sufficient to adversely affect

corn earworm, fall armyworm, and European corn borer ( ~ 2 5 ng

0 g-l) were

much higher than allowed as a contaminant of corn as a feed grain (20 ng g-I).

The toxicity occurs at such a high concentration that it may be of little practical


Maize weevils have greater tolerance to aflatoxin than the lepidopterous insects and can survive on grain with contamination levels exceeding 1 Fg g-1

(McMillian et al., 1981). Corn earworm and fall armyworm have lower tolerances to aflatoxin but, as with the maize weevil, they are more drastically

affected by A. parasiticus isolates and their toxins than those of A. flavus (Wilson

et ul., 1984). Iowa investigators determined that the tolerance of European corn

borers increased with each successive instar, and concluded that levels of toxin

generated under field conditions might occasionally be great enough to adversely

affect the insect, but that the overall influence on the insect population would be

minimal (Jarvis et al., 1984).

As with diseases, the ultimate insect control method is host plant resistance.

The best sources of resistance to various insects will probably be the best option

for control, in that neither plant resistance nor insecticides have eliminated

damage and that plant resistance is the more cost efficient and environmentally

sound. Some resistant germplasm is available for most ear-feeding insects of

importance to corn (Guthrie et al., 1970; Guthrie and Dicke, 1972; Scott and

Davis, 1981; McMillian et al., 1982b; Widstrom et al., 1983, 1992).




Close periodic observations of the corn crop during the early stages of growth

and again during the grain-fill period may be critical to minimizing the risk of



eventual aflatoxin contamination. Anything that induces plant stress (moisture

deficit, insect infestations, disease incidence, or nutritional deficiency) must be

remedied as soon as possible, to prevent the need for lengthy recovery, which

provides a wider window of opportunity for vulnerability to attack by Aspergilli.

Good management is one of the most important components of producing an

aflatoxin-free corn crop, and at worst, a crop with limited contamination in the

most stressful environments. With respect to plant stress, those practices that

maintain the healthiest highly productive plants also minimize aflatoxin contamination.

The growers who maintain good records on crops that were grown in each of

their fields and on problems that were encountered during the cropping history of

those fields are better able to anticipate problems and take steps to avoid them

when corn is again planted in the rotation. A typical example of such records

would be a field map showing those areas that are droughty and have produced

corn with high levels of aflatoxin in previous years. When droughty areas cannot

be avoided, more intensive monitoring of them may serve as an early warning

system to determine when conditions are favorable for aflatoxin development.

Once these areas are identified, they may be either avoided or eliminated from

the harvest when aflatoxin has been detected during years of marginal contamination.


Fortunately, rules for harvest management change very little, whether or not

considerations are made for control of aflatoxin Contamination. The basic tenet is

to harvest the crop as soon as possible after physiological maturity to maintain

grain quality and minimize other losses. The major expense variable at harvest is

the consideration concerning artificial drying. This consideration is often a function of weather, especially temperature and moisture, and ultimately the most

critical decision to be made for control of aflatoxin once the crop reaches maturity.




Early or prompt harvest at maturity is critical in obtaining a crop with minimal

aflatoxin Contamination. Delaying the harvest of a crop which is known to have

some contamination can only result in higher amounts of aflatoxin in the harvested grain (Jones e? d.,

1981). Since contamination is cumulative, delay can

only exacerbate the problem on infected ears, even when some resistance to

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