Taken together, our data showed that prior breastfeeding experience was associated with increases in current complaints of subjective joint pain and diagnostic rates (by radiography) of knee OA in Korean women aged ≥50. In addition, we found that the prevalence of joint pain significantly increased with a breastfeeding duration longer than 25 months.
In this study, longer breastfeeding duration was clearly associated with higher mean age. OA is greatly influenced by age [20]. Hence, during logistic regression analysis, age was the primary factor adjusted for, and participants aged ≥60 were separated and included in a sub-analysis. The results showed greater OR between breastfeeding duration and joint pain and knee OA. When compared with the total participants aged ≥50 years, the OR of knee OA in the breastfeeding groups aged ≥60 years increased from 1.49 to 2.61 (Tables 2, 4). The OR of knee OA was 1.92 in the breastfeeding groups aged ≥50 and 2.75 in the breastfeeding groups aged ≥60, showing a marked increase in older participants (Tables 3, 5).
The effects of breastfeeding on OA have not been fully elucidated. Park’s study (2017) was the first investigation of the association between breastfeeding and OA [3]. It analyzed 6,783 women aged ≥50 years using 1999–2012 National Health and Nutrition Examination Survey (NHANES) data and showed an association between breastfeeding experience of >1 month and an increased risk of OA in older women. In that study, Park considered the “intensity of activities” that induces arthritis in detail. However, variables related to exposure to female hormones that are considered risk factors of OA in women with breastfeeding experience, such as number of pregnancies and number of children, did not show a significant association with the increased risk of OA, and breastfeeding duration could not be determined from the NHANES data.
Until recently, studies on the effects of accumulated breastfeeding duration on the musculoskeletal system in women after menopause have mainly focused on changes in bone density and rheumatoid arthritis. There is still controversy over the association of breastfeeding with bone density [21]. Some studies reported that the bone density of women who are breastfeeding or have just finished breastfeeding is higher than that of non-breastfeeding women [22, 23]. However, other studies investigating bone density among postmenopausal women showed a higher incidence of osteoporosis in those with long-term breastfeeding experience [24]. In a cohort study on 500 women aged 35–55 years, long-term breastfeeding showed significant associations with a decrease in spine bone mineral density after menopause [25].
Numerous studies have reported a negative association between breastfeeding and rheumatoid arthritis. A cohort study of 121,700 women from the Nurses’ Health Study showed that the relative risk of rheumatoid arthritis was significantly lower in those with longer breastfeeding durations [15]. In a cohort study of 18,326 participants from Sweden, the administration of oral birth control pills was not found to lower the risk of rheumatoid arthritis, but breastfeeding did, in proportion to its duration [26].
There are various risk factors for knee OA, such as old age, female sex, high level of activities, consistent exercise, past knee joint injuries, and obesity [20]. In middle-aged or older women in particular, age and female hormone deficiency can simultaneously act as risk factors of joint degeneration [10]. Estrogen deficiency is also associated with OA in humans and animals [27]. Estrogen receptors are present in several cells in the joints, including cartilage cells, subchondral bone cells, and synovial cells, and the expression of estrogen receptors increases in OA patients [27-29]. Experiments using ovariectomized animal models showed that a continued state of low estrogen concentration leads to decreased intra-articular subchondral bone mass, increased interface of the subchondral cavity, and progression of severe cartilage degradation [30]. Altogether, women experience rapid joint degeneration around the ages of 50–75 years after menopause, and show higher prevalence, frequency, and severity of OA than men [9, 20].
Estrogen levels decrease in postmenopausal women, who often complain of muscle pain and joint pain [31]. Compared with the level in men, the estrogen level in women is 3 to 10 times higher. Changes in female hormone levels due to menstrual cycles or menopause, etc. are associated with the increase in mu-opioid receptors related to the female hormone-mediated neurotransmitters for the alleviation of intracerebral pain and perception to pain, and subsequent recall of the pain experience [32]. As a result, this has been reported to induce a higher level of temporomandibular disorders (TMDs), fibromyalgia syndrome (FMS), and migraine in women than in men [32]. In particular, in patients with migraine, it has been found that a rapid decrease in estrogen, which occurs at the beginning of the menstruation period, further increases muscle pain and joint pain, leading to periodic occurrence of headaches [33]. Also, it has been reported that when hormone replacement therapy for postmenopausal women was discontinued, there were occurrences of muscle pain and joint pain [34].
Changes in female hormones after childbirth are partially similar to the changes noted after menopause. Estradiol, which is secreted from the placenta and increases up to 100-fold during pregnancy, instantaneously decreases during childbirth along with placenta extraction, and its concentration is maintained at a low level during breastfeeding as ovulation is delayed [12]. Hence, extended breastfeeding leads to long-term estrogen deficiency [12]. The level of female hormones increases during pregnancy, but breastfeeding can be associated with sex hormone deficiency for several years after childbirth [35]. As a result, low levels of estrogen in breastfeeding women end with the recovery of ovarian function with delactation, but it can be inferred that they have a longer period of undergoing degenerative changes in joints, such as apoptosis of osteocytes and chondrocytes, or hypertrophy of chondrocytes, creating an intracerebral environment that is more sensitive to pain detection compared with non-breastfeeding women or women with short breastfeeding experience.
The long-term breastfeeding experience in a high percentage of Korean women aged ≥60 or older can be attributed to historical and cultural circumstances in Korea. According to a breastfeeding status survey conducted by the Korea Institute for Health and Social Affairs, the breastfeeding rate was 95% in the 1960s and rapidly decreased to 46–68.9% in the 1970s [36]. In the 1960s and 1970s, when women who are currently in their 60s and 70s were likely experiencing childbirth and breastfeeding, Korea was going through rapid economic development after the Korean war, and breast milk supplements were not yet widely marketed [37]. Thus, the period before extensive economic development and the growth of the formula market likely affected long-term breastfeeding among those aged ≥60. Furthermore, the rapid transition from an extended family to nuclear family and a declining birthrate caused by rapid industrialization and modernization are also speculated to have decreased the number of children and lifetime breastfeeding duration among this cohort [38]. Since cultural characteristics such as a sedentary lifestyle in Korea can affect the prevalence of OA in the elderly population, different outcomes might be obtained in different sample groups in the future.
This study has several strengths. To our knowledge, this study is the first to investigate the association between breastfeeding duration and the prevalence of knee OA. Joint pain in old age is a strong indicator of degenerative OA, but at the same time, there are limitations that the individual perception and expression of discomfort vary widely, and the mechanism of pain also differs by individual. OA findings through X-ray are objective and basic tests for determining skeletal status and have clinical significance, but because they do not necessarily involve pain, they cannot serve as the absolute standard for application of clinical treatment by themselves [19]. This study adopted a comprehensive approach to the clinical diagnosis of degenerative knee OA by analyzing joint pain, the subjective symptom, as a dependent variable, and subdividing the disease through knee X-ray images at the same time. The self-administered questionnaire answered by participants was systematically created by skilled experts, and the study was conducted among a large-scale group representative of Korea. In addition, various confounding variables that can affect breastfeeding and the onset of joint pain and OA were adjusted for.
The study also has some limitations. This was a cross-sectional study collecting two data variables from the same period. Thus, only the association between the two variables could be determined and the cause-and-effect relationship could not, in principle, be deduced. However, as breastfeeding is often experienced by women in their 20s and 30s and OA increases on aging, it can be speculated that breastfeeding affects the onset of OA. A sensitivity analysis was additionally conducted on the older participants aged ≥60 years, who had longer duration of breastfeeding and higher prevalence of degenerative OA, and because of the epidemiological structure that prevalence increases for those aged ≥ 50 years, the sensitivity analysis itself, which is limited to those aged ≥ 60 years, may also have limitations.
The data used in this study were responses from self-administered questionnaires, and there could be individual response errors due to the nature of the survey. Additionally, as the study participants were women aged ≥50 years, their memory of breastfeeding from decades ago might have been biased. The social atmosphere that encourages breastfeeding may cause a socially desirable response (SDR) bias in which the memory is biased or exaggerated as if they had breastfed even for women with no experience of breastfeeding or those with short-term breastfeeding, and this bias must be considered in the analysis of the results [39]. However, in this survey, health behavior items such as smoking, alcohol consumption, physical activity, and breastfeeding were surveyed in a self-administered form, not in interview form, and the content of the questions was also written in a fact-oriented manner excluding value judgment. Therefore, it may be expected that SDR bias was minimized in the survey [40].
Individual differences in the subjective perception of joint pain may have also existed. Using the response in the survey, it was defined that “If the subject has felt the pain for 30 days or longer in the last 3 months, the person has joint pain.” This is a characteristic of studies utilizing the KNHANES database, and there is a limitation of not being able to reflect the various levels of pain intensity and frequency of the total population.
Despite the findings of this study, breastfeeding has species-specific superiority as a source of nutrients and immune factors that existing breastmilk substitutes cannot surpass, and it has the effect of formation of attachment between mother and infants and preventing long-term and short-term disease. Therefore, breastfeeding should not be excluded unconditionally as a result of this study, and additional research should be undertaken carefully in other cultures and races.