Male breeding soundness examination (BSE) has become common practice in all domestic animal species. This examination is meant to forecast the ability of a male to impregnate a given number of females within a defined period of time. It is not a fertility test because many males that do not meet the requirements set for the BSE may not be completely sterile and can even impregnate a large number of females under some specific management conditions (Ott and Memon, 1980; Gouletsou and Fthenakis, 2010; Rowe, 2010; Ridler et al., 2012; Van Metre et al., 2012).

In small ruminants BSE is best performed 2 months before the breeding season as part of a flock health visit. About 10% of rams have poor fertility. Many of these can be detected by palpation of testicles without the need for electroejaculation although there are some conditions that are missed if examination of fresh semen is not carried out. The present paper describes an approach commonly used for BSE in rams and bucks. An emphasis is placed on health, physical and sperm abnormalities warranting culling of rams and bucks from reproduction.

Outside of the breeding season (before June in Morocco), the size of testicles and numbers of spermatozoa are lower, especially in breeds with a short breeding season. The testicles should be of similar size, very resilient (turgid) and move freely in the scrotum (compare with others of the same age and similar breed). If the history and examination of the ram and semen show reduced fertility, treatment is not normally possible. A potentially valuable ram may be tested again 2 months later, as infertility is occasionally temporary. The only final evidence of fertility is the production of lambs (Ridler et al., 2012).

Seminal characteristics are highly correlated with the ability to impregnate ewes and semen evaluation can identify most rams of low fertility. A scoring system based on the quantity and quality of semen obtained by artificial vagina can be used. Actual fertility (conception rates) obtained from rams with different semen scores was verified in breeding trials. Synchronized ewes were bred to rams and slaughtered 25 days later to determine conception rates (presence of embryos). The results of these trials showed that 96 to 97% of the rams with semen scores of 3 to 5 had a conception rate of 80 to 100% whereas only 35 and 25 % of rams with scores 2 and 1, respectively, could settle more than 80 % of the ewes (Hulet, 1977; Kimberling, 1984).

A high correlation was found between some semen parameters and fertility or fecundity. In fact, the percentage of live normal spermatozoa, motility, pH and abnormal heads or mid-pieces were the most correlated with fertility (>60 %). Correlation between fecundity and semen parameters was highest for the percentage of live normal spermatozoa, % abnormal necks and % abnormal mid-piece (33 to 44 %) (Hulet, 1977; Kimberling, 1984).

Under natural mating conditions, the reproductive performance of rams can be affected by several factors. These can be grouped into 3 large categories: 1) Factors affecting sperm production, 2) Factors affecting semen quality and 3) Factors affecting the delivery of semen to the female.

The objective of the BSE is to evaluate a male based on its ability to produce and deliver semen in sufficient quantity and achieve high conception rate and fecundity.

The number of spermatozoa produced on a daily basis is directly correlated with the amount of healthy testicular parenchyma (volume or weight). In practice, estimation of the volume or weight of the testis can easily be obtained by measurement of the scrotal circumference at the largest diameter (Braun et al., 1980; Burfening and Rossi, 1992; Elmaz et al., 2007). Thus, this parameter has become an important part of the BSE in males. Minimum acceptable scrotal circumferences for a breeding ram have been set for two groups of ages: Rams less than 14 months old and rams older than 14 months.

Sperm production is also affected by sexual activity, season, nutrition and general health of the ram (Mickelsen et al., 1982; Ahmad and Noakes, 1995; Avdi et al., 2004; Ridler et al., 2012). It is important to conduct a thorough physical examination and evaluation of the body condition of the ram as part of the BSE (Table 1). Ram BSE should be conducted 30 to 60 days before joining, preferably during the natural breeding season and on sexually rested rams. Outside the breeding season or after intensive use, rams will have generally smaller and softer testicles.

Semen quality can be affected during spermatogenesis or during epididymal maturation and storage (Mickelsen et al., 1981; Gouletsou and Fthenakis, 2010; Van Metre et al., 2012). Any disease that may disturb thermoregulation of the testicles or epididymal transit will affect the morphology of the spermatozoa and the fertilizing ability of semen. These factors include systemic diseases, fever or pathological processes at the level of the scrotum, testis or epididymis. It is therefore important to know how to examine and recognize abnormalities or lesions of this part of the genital organs (Table 2).

The most common genital pathology in rams is contagious epididymitis (Figure 11). There are two separates entities in terms of etiology depending on age of the ram: Ram epididymitis (old rams) and lamb epididymitis (virgin rams).

Ram epididymitis is primarily due to Brucella ovis and is probably the most common disease that affects breeding rams. Systematic culling of rams with epididymitis improves flock lambing rates by 10 to 15 %. Bilaterally affected rams are usually sterile but some may retain some fertility (up to 40%). Unilaterally affected males will lose about half of their fertilizing ability (Van Metre et al., 2012; Picard-Hagen et al., 2015).

The primary route of infection in breeding males is the oral or ocular mucous membrane. Homosexual behavior, oral ingestion, genito-nasal investigation amongst rams or ram/ewes are suspected to be the primary mechanisms of transmission. Venereal transmission to ewes is possible. Vertical transmission from ewes to male lambs by transplacental crossing or via milk has been suggested (Ridler and West, 2011; Picard-Hagen et al., 2015).

The organism causes hyperplasia of reticuloendothelial cells, septicemia, and localizes in the epididymis, seminal vesicles, bulbourethral glands and ampullae of the vas deferens, resulting in gross lesions (epididymitis and local interstitial swelling) with plasmocytic and lymphocytic infiltration in the perivascular regions and migration of polymorphonuclear leukocytes (PMN’s) into the epididymal lumen. Ductal epithelial cells undergo hyperplasia in response to the inflammation and form obstructing folds into the lumen as well as mural cysts. Spermatozoa accumulate proximal to the obstruction and eventually cause a rupture of the duct and extravasation of sperm cells into the interstitial tissue and development of granulomas (Carvalho et al., 2012). Pressure from the obstruction leads to degeneration of the seminiferous tissue and testicular atrophy.

Figure 12: Postmortem gross lesion of epididymitis due to B. ovis

Semen quality may start to deteriorate within 2 to 3 weeks of infection. Ejaculate abnormalities consist of decreased motility, decreased sperm concentration and increased number of spermatozoa with detached heads (Table 3) (Cameron and Lauerman, 1976; Kimberling et al., 1986; McLaren, 1988). In addition to epididymitis other differential diagnoses of increased scrotal size (i.e. swelling) include:

Inguinal hernia with omentum extending through the inguinal ring.

• Edema of the scrotal skin.

• Hematoma.

• Orchitis.

• Hydrocele.

• Varicocele.

• Spermatocele.

• Puncture wound causing cellulitis.

Infected rams can be detected by serology. Complement fixation test (CF) is usually positive within 6 to 9 weeks of infection (titer 1:160 or greater) and remains elevated for up to 7 months or longer. CF is a screening test but lacks sensitivity and specificity (too many false negative and false positive results). An ELISA test is more sensitive and false positives are generally not a problem. ELISA is also useful in the early detection of the disease (Ridler and West, 2011; Franca et al., 2014; Ridler et al., 2014).

Lamb epididymitis is caused primarily by Actinobacillus seminis (Heath et al., 1991). It affects rams at pre-breeding age, particularly those that are on high plane of nutrition. The infection in a group of ram lambs is spread by oral-nasal contact with urine of preputial secretion during the typical prepuce investigation behavior displayed by rams. Ascending infection has also been incriminated. Prevention of the disease by vaccination or prophylactic antibiotics is of limited value. Some lambs with high PMN’s have been treated successfully with long acting tetracycline (20 mg/kg). Actinobacillus seminis was isolated from rams with abnormal semen or fertility. In one study (Al-Katib and Dennis, 2005), clinical signs were not always present although two of five experimentally infected rams presented palpable lesions. Necrotic testicular and epididymal abscesses may be seen on postmortem examination. A. seminis was isolated from seminal vesicles and epididymis of a ram with no gross lesions. This suggests that A. seminis infection may be widespread and should be considered in cases of infertility (Mbai et al., 1996; Al-Katib and Dennis, 2005; Otter, 2008; Al-Katib and Dennis 2009; Gouletsou and Fthenakis, 2015; Acosta-Dibarrat et al., 2016).

Control of ram epididymitis in a flock rests mainly on periodic examination of rams and strict enforcement of guidelines for scrotal palpation, scrotal circumference, semen quality and ELISA testing. In most breeds, all ram lambs with less than 30 cm scrotal circumference or abnormal testicular consistency should be culled from breeding. In geographical areas where the disease is endemic, rams should also be evaluated after the breeding season. Vaccination may be used as an adjunct control method. However, vaccinated rams cannot be serologically tested. In this case, semen culture is needed to identify infected rams. Vaccination may be performed twice a year, pre-breeding and after the breeding season. (Ridler and West, 2011; Picard-Hagen et al., 2015).

A stricter control program consists of performing a BSE on all rams in addition to serology and semen culture. Rams should be tested at pre-breeding exam and 30 to 60 days after the joining period. All rams with abnormal semen parameters, small scrotal circumference or suspected of having epididymis or are positive to the ELISA should be immediately culled (Ridler and West, 2011).

In flocks where brucellosis is already present, eradication can be accomplished using one of several management approaches based on testing and culling infected rams and avoiding the introduction of new infected animals. In the initial part of the program, rams should be tested frequently (at 30 to 60 day interval) in order to detect rams that may have been incubating the disease but were not serologically positive.

All positive or suspect rams should be culled and replaced by negative virgin ram lambs. Leasing or exchanging rams should be discouraged unless the other flocks have the same eradication program.

Eradication of brucellosis can be achieved gradually in larger flocks by first establishing two flocks: a “clean” and an “infected” flock with strict separation. Clean rams are used on separate ewes and should be tested at the end of each breeding season. Replacement for the clean flock must be ELISA negative, and rested for 30 days after purchase. As the incidence of infection is reduced in the clean flock and the natural attrition decreases infected flock numbers, a total eradication program can be initiated.

The most important factors that play a role in the ability of the ram to deliver semen to ewes are physical unsoundness, libido and management conditions (Toe et al., 1994; Gouletsou and Fthenakis, 2010; Menegassi et al., 2012; Smith et al., 2012; Van Metre et al., 2012). Physical problems such as lameness, blindness (Table 1) and penile or preputial problems (Table 2) may not interfere with semen production or quality but rams will not be able to find estrous ewes and/or mate them, resulting in poor reproductive performance.

Libido (mating ability or serving capacity) is another factor that affects the reproductive capacity of the ram (Alexander et al., 2012). Unfortunately, this is not evaluated during the routine examination of the ram. It is very important to be able to track ram sexual activity after joining and identify rams with poor serving capacity. This is easily done if the ram is fitted with a marking harness. This management procedure will allow the breeder to also monitor sexual activity in ewes and the number of ewes returning to estrus. Monitoring of serving capacity is critical when using young virgin rams because of their lack of experience.

Ram to ewe ratio should be adjusted for each management condition according to the following general guidelines:

• 1 ram to 50 ewes for paddock mating (mature rams)

• 1 ram to 25 ewes for paddock mating (young rams)

• 1 ram to 30 ewes for mating in rough terrain

• 1 ram to 15 ewes for synchronized flock

• 1 ram to 10 ewes for out of season breeding

The current Society for Theriogenology (SFT) guidelines for BSE emphasize the general health, physical examination (Tables 1 and 2), scrotal circumference (Figure 15), sperm morphology and motility. Ejaculates are collected most commonly by electroejaculation (Figure 16). The semen samples should be protected from cold shock in order to evaluate motility (Figure 17). The characteristics of the normal ram ejaculate are summarized in Table 4. Determination of sperm concentration is not usually performed in the field. However, the gross appearance of the ejaculate may be used as an estimate (Table 5) (Figure 18). Motility can be evaluated grossly (wave like motion) on a non-diluted sample without cover slip (x 100). Individual motility may be performed on a cover-slipped sample after dilution of semen with an appropriate semen extender (x 200 x 400) (Table 6). Sperm morphology should always be performed under oil (x 1000). Various staining techniques are available but the most common is eosin-nigrosin staining procedure (Figures 19, 20, 21, 22). The main abnormalities that are often missed by practitioners are head (vacuoles, diadems), acrosomal defects (folded or knobbed) (Figure23) and other cells (spheroids, medusa cells) (Figure 24). Observation under phase contrast microscopy of a fixed sample is useful for characterization of some head and acrosomal defects (Figure 26). Diffquick® or Giemsa staining techniques are helpful in identifying spheroids and white blood cells (Figure 24).

Ultrasonography of the scrotum and its content may be indicated in some cases and is discussed in detail in a separate article (Boukhliq et al., 2018). This technique allows visualization of lesions that may not be palpable. Sperm granuloma or spermatic granuloma results from extravasation of spermatozoa into the interstitium of the organ. Expect for the granulomatous reaction, they are microscopically similar to spermatocele. Sperm granulomas (Figure 14) and spermatoceles (localized accumulation of spermatozoa within a dilated epididymal or testicular duct) are common and may be non-infectious due to blind efferent tubules and segmental aplasia of the Wollfian duct.

Figure 15: Scrotal circumference measurement is performed using a measuring tape at the largest diameter including both testicles

Epididymal granulomas in the caput and cauda epididymis are seen as anechoic or hyperechoic areas with a distinct margin with or without a hyperechoic capsule. Granulomas of the testis are generally microscopic and do not appear on ultrasound. Enlargement of the mediastinum testis is detected when granulomas are present in the head of the epididymis. Heterogeneous testicular parenchyma with presence of numerous hyperechoic foci is typical for testicular degeneration associated with testicular and epididymal granulomas.

Rams are classified based on physical examination and semen evaluation finding in one of 4 categories: Unsatisfactory, questionable, satisfactory, and excellent.

The Unsatisfactory ram

A ram is classified as unsatisfactory if it fails to meet the minimum requirements for any one part of the examination. Normally, these rams should be culled from the breeding program. However, if there are no infectious problems and the veterinarian thinks that the changes are reversible, the option to retest the ram should be given to the owner. Unsatisfactory category will include rams with the following:

• Severe health problems, congenital abnormalities, bad conformation.

• Cryptorchidism, hernias, epididymitis, scrotal abscess, severe balanoposthitis (“pizzle rot”), penile adhesion, very soft testicles, lumps or scrotal swelling, orchitis, testicular hypoplasia, marked difference in size between the testicles.

• Scrotal circumference: Less than 30 cm for lambs or less than 33 cm for rams

• Sperm morphology: > 50 % abnormalities

• Sperm motility: < 30 %

• Positive ELISA test for B. ovis (should be done on all range rams and rams over 9 months of age)

• Clinical signs: Depression, fever, pink eye, foot rot, lameness, bluetongue, sore mouth, ring worm, other contagious diseases would render the ram either unsatisfactory or questionable.

The Questionable ram

This category includes all rams with one questionable parameter or suffering from a treatable or reversible condition. These rams may be used in a limited breeding program if they do not have any contagious disease. Questionable rams should be retested within 50 to 60 days after implementation of treatment and re-classified as satisfactory or unsatisfactory breeders. Common reasons for classifying a ram as questionable include:

• Body condition score: Under-conditioned (1 or 2) or over-conditioned (5).

Figure 19: Morphological abnormalities of the sperm head (eosin-nigrosin stain)

• Mild to moderate balanoposthitis, scrotal dermatitis, frost bite, mange.

• Scrotal circumference: less than 30 cm for lambs or less than 33 cm for rams.

• Sperm morphology: >30% abnormalities.

• Sperm motility: < 30%.

• Suspect ELISA test for B. ovis, retest in 30 to 60 days.

The Satisfactory ram

This category includes rams that meet all the minimum requirements for general health, scrotal circumference, sperm motility and morphology. These rams will achieve good reproductive performance if joined to ewes at a ratio of 1:50 for 60 days. They should fulfill the following requirements:

• Good general health

• Good conformation

• Normal genital tract

• No previous history of infertility

• Body condition score of 3 to 4

• Scrotal circumference: 30 cm or more for <14 months of age, 33 cm or more for 14 months or older

• Sperm morphology: ≥70 % normal

• Sperm motility: ≥30 % progressive motility

• ELISA negative for B. ovis.

Figure 20: Morphological abnormalities of the midpiece and tail (esosin-nigrosin stain)

The Excellent ram

This category includes rams that meet more stringent requirements for scrotal circumference, motility and morphology. Exceptional rams are expected to achieve good reproductive performance at a ratio of 1 ram to 100 ewes. They should have the following attributes:

• Excellent health

• BCS, 3 to 4

• Scrotal circumference: more than 33 for less than 14 months old and more than 35 for 14 months or older

• Sperm morphology: ≥ 90 % normal

• Sperm motility: > 50 % progressive

• ELISA negative for B. ovis

There are no specific guidelines for BSE in the male goat (Ott and Memon, 1980; Al-Ghalban et al., 2004; Rowe, 2010; Ridler et al., 2012). Most practitioners use the same approach described for rams. Bucks should ideally be tested for Corynebacterium pseudotuberculosis and Caprine arthritis-encephalitis virus (CAEV). It is important to remind clients that bucks should be purchased from reputable breeders with sound biosecurity and preventive herd health program. Bucks should be examined for gastrointestinal parasites particularly if they come from areas where there is a problem of anthelmintic resistance. If arthritis is due to CAEV, the buck should be eliminated from reproduction because of the increased susceptibility of his daughters to the same disease. Common abnormalities of the genital organs are summarized in Table 7.

Scrotal circumference should be at least 25 cm for breeds weighing more than 40 kg (Figure 27). Most dairy breed bucks have SC of 25 to 28 cm when they reach 45 kg of body weight. Dairy bucks may be as early as 7 months of age. Meat breed bucks have a SC of 26 to 29 cm around 7 months of age (45 kg BW) (Almeida et al., 2007; Rowe, 2010).

Semen can be collected by electroejaculation, however the owner should be warned that goat tends to vocalize a lot and that this procedure may be better done under sedation. The authors prefer to collect bucks using and artificial vagina, which is readily accepted when in presence of an estrous doe. Non-estrous does have also been used successfully. In general, a buck is deemed satisfactory breeder if he passes the physical examination, and has an ejaculate with at least 50 % progressively motile spermatozoa and less than 30 % total sperm abnormalities (Rowe, 2010; Ridler et al., 2012). Some bucks may produce yellow ejaculates (Figure 28). This is due to a genetic ability to produce and concentrate large amounts of riboflavin. This character does not affect fertility (Mendoza et al., 1989).

It is estimated that 3.5 to 10 % of ram population will not pass the breeding soundness examination. In a retrospective study on 14,667 BSEs on rams in the western USA, 29% of the examined animals failed (Van Metre et al., 2012). The most common reason for failure was poor semen quality (43.8% of failures), which emphasizes the importance of adequate preparation and examination of semen samples. Inflammatory causes, physical abnormalities and emaciation were the cause of failure in 20 %, 15.5% and 14.2 %, respectively. In the same study, the seroprevalence of B. ovis was 10.0 % and seropositive status was not associated with poor semen quality in several cases which emphasize the importance of serologic testing. In another study in Spain, 16.7 % of examined rams (n = 897) were classified as unsuitable based solely on clinical examination (Mozo et al., 2015). The primary cause of failure in that study were ulcerative posthitis and testicular lesions. Breeding soundness examination of rams and bucks is an important veterinary service to sheep and goat producers. Not only it can greatly impact fertility but also it reduces chance of introduction of contagious or hereditary diseases in the herd of flock.

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