The Common Clinical Signs and Pathological Lesions of Mycotoxicoses in Poultry

Introduction

Poultry feed production and cost are major issues faced by poultry industries in many countries of the world. Grains, such as corn, wheat, soybean, rice and their by-products used for the production of poultry feed are shared by humans and animals. Due to the competitive pricing of raw material and their availability on the market, sometimes lower quality feed ingredients are used in poultry feed production. These materials may be stored for longer periods and due to poor storage conditions, they may be contaminated with fungi, especially in humid and hotter countries, such as Indonesia. Some fungi may produce mycotoxins as secondary metabolites that further contaminate these grains used for feed ingredients.

Mycotoxicoses is a general term for toxic and/or carcinogenic diseases caused by ingestion, inhalation, or direct contact of feed contaminated with one or more mycotoxins. These diseases may vary on the severity, target sites, and mechanism of toxicity. The severity of the disease condition varies in type and dose of mycotoxins as well as the duration and frequency of contact with mycotoxin/mycotoxins. Poultry ingesting mycotoxin in high concentration may likely suffer from acute or sub-acute disease where toxic effects directly affect specific tissues or organs. However, mycotoxicoses in lower levels with continued introduction of mycotoxins may cause chronic disease, which may further worsen by secondary infections due to their immune suppressive effects (Naehrer, 2012). Specific mycotoxins affect various organs and/or tissues, such as the liver, kidneys, brain, mucous membrane of the gastrointestinal, respiratory tract, reproductive and urogenital system, and skin (Devegowda and Murthy, 2005).

Mycotoxicoses should be differentiated from mycoses which are systemic diseases caused by invasion of growing fungi into living tissues, initiating mechanical destruction.

Mycotoxins are a group of structurally diverse toxic and/or carcinogenic chemical compounds produced by certain fungi as secondary metabolites as a result of their organic processes. They are synthesized and excreted during the maximum growth of certain fungi under favorable conditions (Naehrer, 2012). Most mycotoxins are known to hazardously contaminate crops and consequently poultry feeds and poultry products, causing significant economic losses associated with their impact on poultry and human health, poultry performance, and domestic as well as international trade.

This paper presents the common clinical signs and pathological lesions caused by the most important mycotoxins in the poultry industry in Indonesia.

Characteristics of mycotoxins

Mycotoxins are chemical compounds of low molecular weight and low immunogenic capacity. They are chemically stable due to their chemical structure and low molecular weight. They resist high temperatures, remain stable during storage and during feed processing conditions (Bullerman and Bianchini, 2007). Mycotoxins carried over at low levels, such as aflatoxins, ochratoxins, T-2 toxins can be found in the liver, kidney, muscle, and eggs CAST, 2003, Volkel et al., 2011). At some extent, they may be a potential risk to consumers of food products of poultry origin (Naehrer, 2012).

Mycotoxin contamination and the severity of the problem caused by these compounds vary from year to year and also from one geographic region to the other. Many fungi contaminate the crop during the growing season and others are seed borne and grow along with the plants, whereas others infect commodities during storage. Contamination and subsequent mycotoxin production may be influenced by the environmental conditions at specific times during the crop development or storage (Sanchis, 2004). Therefore, the formation of mycotoxins in the field is difficult to control. As stated by Park and Stoloff (1989) “Mycotoxin contamination is unavoidable and unpredictable, which makes it a unique challenge to food and feed safety”. The FAO has estimated that up to 25% of the world’s food are significantly contaminated with mycotoxins (Adams and Motarjemi, 1999). However, genetic and breeding studies may eventually provide for obtaining resistant or non-susceptible varieties of certain commodities for fungal contamination and/or mycotoxin formation.

The only proven way to determine, if grains contain mycotoxins or not, is to test for them in the laboratory. However, contamination with mycotoxins can be suspected if certain signs or characteristics appear in the raw materials for feed. Such signs may be visually discolored kernels, musty odor, lighter weight than usually kernels, or with wrinkle kernels in grain (Richard, 2012). Several hundreds of mycotoxins have been reported and isolated, as many as approximately 400 varieties, with their target sites and toxicity, with varying chemical structures of each one. In the poultry industry, mycotoxins that cause the most economic impacts on poultry production are afltoxins (Afla), trichothecenes (namely T-2 toxin, T-2; deoxynivalenol, DON), ochratoxin A (OTA), fumonisins (FUM), zearalenone (ZEN), and ergot alkaloids (Ergots) (Jelinek et al., 1989, CAST, 2003, Naehrer, 2012).

Mechanisms of mycotoxins toxicity

The mechanisms of mycotoxins toxicity are not fully understood due to the diversity in their chemical structures and target organs. Ochratoxin A, T-2 toxin, aflatoxin B1 may inhibit the synthesis of DNA, RNA, and protein and may damage DNA. Most mycotoxins can cause lipid peroxidation, damage of membrane structures and their functions, induces apoptosis (programmed cell death) leading to cellular necrosis (Surai, 2002, Fink-Gremmels, 2008). The mycotoxins may cause immune suppression (impairment of immune system), hepatotoxicity (damage to the liver), nephrotoxicity (damage to the kidneys), neurotoxicity (damage to the central and peripheral nervous systems), genotoxicity (damage to DNA leading to cell transformation, abnormal cellular proliferation and finally tumor formation) (Devegowda and Murthy, 2005, Tabbu, 2015).

Aflatoxicosis

Aflatoxin is known to have a hepatotoxic effect in chickens (Dalvi, 1986, Espada et al., 1992) and also known to have hepatocarcinogenic effect in exposed animals (CAST, 2003).

The common clinical signs related to aflatoxicosis in chickens, include decreased feed intake, poor growth and inhomogeneous flocks (Figure 1), increased mortality, abnormal pigmentation (shank, feet), feed passage, and higher feed conversion rate (FCR). The most consistent findings in chickens suffer from aflatoxicosis was immune suppressive effects, include more susceptible to diseases, decreased responds to vaccination and antibiotic treatment, and decreased resistance to environment stress. In many cases of aflatoxicosis there was an increase in leg problems, leg weakness, reduced bone strength, short shank, and leg deformity. In some cases, there were anemia and abnormal blood clotting, increased incidence of bruising and down grading, and nervous syndrome (abnormal behavior).

The most frequent effects of aflatoxicosis in layers and parent stocks were decreased egg production, reduced egg size, poor (thin) egg shell, pale egg shell and egg yolk. In parent stocks, there was a reduction in fertility and hatchability, increased embryo mortality in the hatchery, and lower semen volume in male parent stocks.

The most common pathological lesions associated with aflatoxicosis in chickens were found in liver, lymphoid organs, and testes (male parent stocks) and the process of this disease was commonly chronic. In acute-subacute aflatoxicosis, the liver appeared enlarged, pale yellow in color, friable, and usually the gall bladder was enlarged and filled with bile. The pancreas was usually small and depigmented and there were hemorrhages on subcutaneous tissues and muscles. In chronic aflatoxicosis, the liver was small, firm, and rounded (Figure 2). Sometimes this organ was very small, rounded, and rubbery which very often complicates with ascites and hydropericardium. The other consistent lesions in aflatoxicosis were found in bursa Fabricius, thymus, and spleen which appeared smaller than normal (Figure 3); in male parent stocks, the size of testes was significantly reduced (Figure 4).

Trichothecenes toxicosis

Trichothecenes mycotoxins affect actively dividing cells, such as those lining the gastrointestinal tracts, skin, lymphoid and erythroid cells. They have caustic and irritant effects on the skin and mucous membrane (Devegowda and Murthy, 2005).

Trichothecenes mycotoxins which are commonly found in the field, include T-2 toxin, diacetoxyscirpenol (DAS), and deoxynivalenol (DON). The common clinical signs related to these mycotoxins were decreased feed intake, included feed refusal or prolonged feed finish, growth depression, inhomogeneous flocks, impaired FCR, immune suppression, poor or abnormal feathering (Figure 5), dermal and oral lesions (crust on the beak, ulcers in oral cavity) (Figure 6). Additional symptoms which were commonly found were diarrhea, abnormal pigmentation, anemia, and rickets effects, including severe fragility and bending of long bones and shanks, soft and bending of beak. In layers and parent stocks, there was a sharp decrease in egg production, poor egg shell, increased number of cracked eggs, reduced egg size; cyanosis of the comb and wattle; decreased fertility and hatchability (parent stocks). Sometimes there were neural disturbances, such as abnormal wing positioning or lack of reflexes.

The common pathological lesions related to trichothecenes mycotoxicoses were crust on the beak, yellow caseous ulcers at the margin of the beak, mucous of the hard palate and the angle between mouth and tongue (Figure 7); ulcers may extend to the esophagus and larynx, gizzard erosion (GE) (Figure 8), atrophy of thymus, bursa Fabricius, and spleen. Other lesions commonly found were hemorrhages on the intestinal mucosa, pale or yellow discoloration of the bone marrow, dermal necrosis, vesicular lesions on the feet and legs, and enlargement of costo-chondral joints (related to rachitic rosary). In layers and parent stocks, there was regression of ovaries and atrophy of oviduct.

Ochratoxicosis

Ochratoxin type mycotoxin which is most commonly found in the field is ochratoxin A (OTA), which has a primary target organ on the kidneys as it is known to be nephrotoxic (Pfohl-Leszkowic and Manderville, 2007). Residues of OTA may be found in liver, kidneys, muscle, and eggs (CAST, 2003) and possess carcinogenic effects, which may be harmful when consumed by humans (Pfohl-Leszkowic and Manderville, 2007).

The common clinical signs related to OTA were decreased feed consumption, decreased weight gain, retarded growth (Figure 9), poor feathering, higher mortality rate, higher FCR, abnormal pigmentation (shank, feet), increased water consumption, and immune suppressive effects. In layers and parent stocks, observations were decreased egg production, egg size, and egg weight; poor egg shell; eggs with blood/meat spots in the yolk or albumin; delay in sexual maturity (Figure 10). In parent stocks, there was a decrease in hatchability and poor progeny performance.

The common pathological lesions related to OTA were seen in the kidneys, which were extremely swollen and pale in color with very distended ureters due to the accumulation of urates (Figure 11); atrophy of bursa Fabricius, thymus, and spleen; and soft or severely fragile of bones. Other common changes were found in eggs, which had watery thin albumin and blood/meat spots on the thick albumin or yolk (Figure 12).

Fumonisins toxicosis

Fumonisin which is most frequently found in the field is fumonisin B1. Poultry are less sensitive to this compound. Fumonisins disrupt sphingolipid metabolism and block the synthesis of complex sphingolipids from sphinganine (Sa) and sphingosine (So). As a consequences, Sa and So accumulate in tissues and their accumulation can be used as a biomarker to indicate fumonisin contamination (Starkl and Naehrer, 2015). Fumonisin B1 is classified as a possible human carcinogen (Group 2B) (IARC, 1993).

The common clinical signs related to fumonisins were severe reduction in feed intake, especially in layers, lowered average daily weight gain, reduced body weight, impaired FCR, increased mortality (sometimes spiking mortality), diarrhea (sometimes dark and sticky excreta were seen) (Figure 13), abnormal pigmentation, immune suppression, and rickets effects. In layers and parent stocks, there were decreases in egg production, lower egg weight, poor egg shell (more brittle), an increased percentage of eggs with small and disintegrated yolks. In parent stocks a decrease in fertility and hatchability were observed.

The common pathological lesions associated with fumonisins were enlargement of proventriculus and ventriculus (Figure 14), gizzard erosion (Figure 15), watery accumulations in the lumen of intestine, sometimes enlargement of pancreas; increased weight of liver, kidneys, and heart; atrophy of bursa Fabricius, thymus, and spleen. Sometimes there were indications of rickets effects, such as enlargement of costo-chondral joints, severe fragility or bending of long bones (Figure 16); soft and bending of beaks and claws.

Zearalenone toxicosis

Since zearalenone is known to be primarily an estrogenic mycotoxin, this toxin appears to bind to estrogenic receptors and results in hormonal changes. Chickens are highly tolerant to zearalenone; therefore high doses are required to cause reproductive disorders. In the field, zearalenone and DON were found simultaneously in feed or raw materials (Richard, 2012), and may have synergistic interaction (Naehrer, 2012).

The common clinical signs associated with zearalenon in layers were decreased egg production, reduced egg specific gravity, poor egg shell and interior egg quality. In parent stocks, reduction in egg production, enlarged abdomen due to cystic oviduct, enhanced secondary sex characteristics and lowered serum progesterone occurred. In broilers, enlargement of comb and wattles (Figure 17), prolapsus of cloaca (Figure 18) were observed.

The common patho­logical lesions related to zearalenon in layers and parent stocks included the prolapsus of oviduct and the enlargement of cloaca. In layer chicks, an enlargement (due to local edema) of bursa Fabricius (Figure 19), cystic on the peritoneal surface (Figure 20) or within the oviduct were identified. In male broilers, there were decreased comb and testes weights, whereas in female broilers, there were increased comb, bursa Faricius, and ovary weights, and enlargement of oviduct.