George Papanicolaou was the first to design a large study evaluating fluid aspirated from the nipple rather than collecting fluid that came forth spontaneously. In his 1958 report evaluating NAF, he stated, "The practicability of utilizing breast secretion smears in screening for mammary carcinoma is in great measure dependent upon obtaining secretion in a relatively large proportion of the female population" (Papanicolaou et al., 1958). He cleansed the nipple and applied gentle massage toward the areola. If NAF did not come forth, he used a breast pump to create mild suction. He reported a series of 917 women without breast complaints in whom he attempted to collect NAF from one or both breasts (Papanicolaou et al., 1958). He was able to obtain a sample in 18.5% of subjects.
In order for NAF to be useful as a screening tool, it is essential to collect a sample in the vast majority of women. As a result, increasing the success rate continued to be an important area of investigation for the next 30 years. Early studies indicated that the ease of collecting NAF was related to the ethnicity of the individual, with NAF being more difficult to collect from Asians than African Americans or Caucasians (Petrakis et al., 1975). This was presumed to be due to the physiology of the breast, a modified ceruminous gland and is probably related to the secretory pattern in the breast and other ceruminous glands, which provide less secretions in most Asians (Petrakis, 1971) and American Indians (Petrakis, 1969) who are thought to have come from Asia than in Caucasians and African Americans. Other variables (Petrakis et al., 1975) found linked to success in NAF collection included age (late premenopause had the highest yield) and menopausal status (premenopausal subjects more often provided NAF). Various nipple aspiration devices were created, notably one by Otto Sartorius (Sartorius et al., 1977), which provided NAF on average in 50 to 60% of subjects (Petrakis et al., 1975; Sartorius et al., 1977) and in up to 80% in the highest-yielding subset of subjects (Sartorius et al., 1977).
The ability to collect NAF was linked not only to age, race, and menopausal status, but also to body habitus. In a large sample of white and black women between the ages of 20 and 59 years old who did not have a history of breast cancer, the proportion of women from whom NAF was collected increased with increasing dietary fat consumption (Lee et al., 1992b). This association of NAF yield with fat consumption was especially strong among black women, and was most pronounced in women aged 30 to 44 years.
In the 1990s the aspiration technique was modified to emphasize warming the breast, breast massage, and multiple aspiration attempts after clearing the nipple of dried secretions (Sauter et al., 1996). Each of these techniques had been heretofore practiced, but the emphasis on persistence seemed to increase successful NAF collection, as did having the subject return for a second or third visit, if necessary, to collect NAF. This increased yield to 99% of subjects who had not undergone prior breast surgery in the subareolar region, and who had not received breast irradiation (Sauter et al., 1996). Others have reported success rates near 90% without repeat visits (Mitchell et al., 2002), and investigators with yields after one visit of 66% increased their yield to 78% with multiple visits (King et al., in press).
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