Throughout the animal kingdom, mothers transfer microbes to their young while giving birth. Different species of tadpoles acquire specific skin bacteria from mother frogs even though they all live in the same pond with the same bacterial background. Emerging chicken eggs get inoculated with microbes from a bacteria-filled pouch near the mother hen’s rectum. And for millennia, mammalian babies have acquired founding populations of microbes by passing through their mothers' vagina. This microbial handoff is also a critical aspect of infant health in humans. Today it is in peril.
Microbes play a hidden role in the course of every pregnancy. During the first trimester, certain species of bacteria become overrepresented while others become less common. By the third trimester, just before the baby is born, even greater shifts occur. These changes, involving scores of species, are not random. The compositions change in the same direction across the dozens of women who have been studied.
Many physiological and pathological features of pregnancy are controlled, at least in part, by the mother’s resident microbes, which evolved to help her and themselves. When food is in short supply during pregnancy, as has often occurred in human history, the mother’s microbes will shift their net metabolism so that more calories flow from food to her body. In this way, her microbes increase the odds that there will be a next generation, one that will provide a new home for them.
Thus shifts in microbial composition may be partially responsible for those extra pounds a mother gains, as well as for the increased sugar or glucose levels that commonly occur during pregnancy. It makes sense; mothers store more energy to optimize the success of their newborns.
As microbes in the mother’s intestinal tract store up energy, another population of microbes—this time in her vagina—begins shifting as well. Women of reproductive age carry bacteria, primarily lactobacilli, which make the vaginal canal more acidic. This environment provides a hardy defense against dangerous bacteria that are sensitive to acid. Lactobacilli also have evolved a potent arsenal of molecules that inhibit or kill other bacteria.
During pregnancy, these tiger-mother lactobacilli flourish, crowding out other resident species and potential invaders. They are gearing up for the main event—birth. When the mother’s water breaks, a rush of fluid is unleashed, sweeping up bacteria as it flows onto her thighs. This splash, now dominated by lactobacilli, rapidly colonizes the mother’s skin.
Whether the birth is fast or slow, the formerly germ-free baby soon comes into contact with the lactobacilli. The baby’s skin is a sponge, taking up the vaginal microbes rubbing against it. The first fluids the baby sucks in contain mom’s microbes, including some fecal matter. Labor is not an antiseptic process, but it has been going on like this for a long time—at least 70 million years since our earliest mammalian ancestors.
>The first fluids a baby sucks in contain its mother's microbes. Labor is not an antiseptic process, but it's been this way for at least 70 million years.
Once born, the baby instinctively reaches his mouth, now full of lactobacilli, toward his mother’s nipple and begins to suck. The birth process introduces lactobacilli to the first milk that goes into the baby. This interaction could not be more perfect.
Lactobacilli and other lactic acid–producing bacteria break down lactose, the major sugar in milk, to make energy. The baby’s first food is a form of milk called colostrum, which contains protective antibodies. The choreography of actions involving vagina, baby, mouth, nipple, and milk ensures that the founding bacteria in the baby’s intestinal tract include species that can digest milk for the baby.
These species are also armed with their own antibiotics that inhibit competing and possibly more dangerous bacteria from colonizing the newborn’s gut. The lactobacilli become the earliest organisms to dominate the infant’s formerly sterile gastrointestinal tract; they are the foundation of the microbial populations that succeed them. The baby now has everything it needs to begin independent life.
Breast milk, when it comes in a few days later, contains carbohydrates, called oligosaccharides, that babies cannot digest. But specific bacteria such as Bifidobacterium infantis, another foundational species in healthy babies, can eat the oligosaccharides. The breast milk is constituted to give favored bacteria a head start against competing bacteria.
Cesarian delivery is a largely unrecognized threat to the microbial handoff from mother to child. Instead of traveling down the birth canal picking up lactobacilli, the baby is surgically extracted from the womb through an incision in the abdominal wall.
When the mother’s or baby’s life is in danger for any reason, emergency C-sections are performed, often with short notice. Physicians also influence their patients’ choices. Some are very conservative when they see any signs of fetal stress or suspect that the mother will have problems. On a more cynical note, it takes less time and fuss to do a C-section than to wait out a vaginal birth. And most doctors and hospitals make more money from performing C-sections than from natural births.
For all of these reasons, U.S. C-section rates increased from fewer than one in five births in 1996 to one in three births in 2011—a 50 percent increase. If this trend continues, half of all U.S. babies (2 million a year) might be delivered surgically by 2020.
>The founding populations of microbes found on C-section infants are not those selected by hundreds of thousands of years of human evolution.
But so what? Why not perform a Cesarian if it makes the mother more comfortable and is easier on the physician, if there is no cost other than the hospital bill? Well, there is a cost—a biological one—and it affects the baby.
A few years ago in Puerto Ayacucho, Venezuela, my wife, Gloria, conducted the first study of its kind to test whether the microbes found on newborn babies delivered vaginally or by C-section varied in any way.
Nine women participated. Four mothers delivered naturally and five had C-sections. Gloria sampled each mom’s skin, mouth, and vaginal microbes one hour before delivery. By DNA sequencing, she showed that the women all had similar proportions of the major bacterial groups present at each site.
Each baby’s skin, mouth, and nose were sampled less than 15 minutes after birth. She sampled their first stool, called meconium, 24 hours later.
The mouths, skin, and first bowel movements of babies born vaginally were populated by their mother’s vaginal microbes: Lactobacillus, Prevotella, or Sneathia species. Those born by C-section harbored bacterial communities found on skin, dominated by Staphylococcus, Corynebacterium, and Propionibacterium.
In other words, their founding microbes bore no relationship to their mother’s vagina or any vagina. At all the sites—mouth, skin, gut—their microbes resembled the pattern on human skin and organisms floating in the air in the surgery room. They were not colonized by their mother’s lactobacilli. The fancy names of these bacteria don’t matter as much as the notion that the founding populations of microbes found on C-section infants are not those selected by hundreds of thousands of years of human evolution or even longer.
Another threat to a baby’s newly acquired resident microbes involves antibiotics given to the mother. Most doctors consider it safe to prescribe penicillins for all sorts of mild infections in pregnancy—coughs, sore throats, urinary tract infections. Sometimes when doctors think that the mother has a viral infection they also give antibiotics just in case it is actually a bacterial infection.
As we know, the antibiotics affect the mother’s resident microbes, inhibiting susceptible bacteria and selecting for resistance. The closer the dose is to birth, the greater the possibility that she will pass a skewed population of microbes to her baby.
Then comes the birth itself. Women in labor routinely get antibiotics to ward off infection after a C-section. Antibiotics are also used to prevent a serious infection in newborns caused by Group B strep, a bacterium that between a quarter and a third of U.S. pregnant women carry. It lives in the gut, mouth, skin, and sometimes the vagina and rarely causes any problem in the mother. But sometimes Group B strep can be lethal to newborns' fragile immune systems. While such infections are uncommon, professional groups recommend that all pregnant women be screened for the microbe near the time of delivery. If they are positive, they get a dose of an antibiotic shortly before the baby descends the birth canal.
>Antibiotics are broad in their effects, not targeted. While they kill Group B strep, they also kill friendly bacteria, thus selecting for resistant ones.
Each year in the United States well over a million pregnant women are Group B strep–positive, and all will get intravenous penicillin during labor to protect their babies. But only one in 200 babies actually gets ill from the Group B strep acquired from his or her mother. To protect one child, we are exposing 199 others to antibiotics.
The problem, of course, is that we know antibiotics are broad in their effects, not targeted. While the antibiotic kills Group B strep, it also kills other often-friendly bacteria, thus selecting for resistant ones. This practice is altering the composition of the mother’s microbes in all compartments of her body just before the intergenerational transfer is slated to begin.
The baby also is affected in similar unintended ways. Any antibiotic that gets into the bloodstream of the fetus or into the mother’s milk will inevitably influence the composition of the baby’s resident microbes, but we are only beginning to understand what this means.
Finally, the babies are directly exposed. Most parents are not aware that all American-born babies today are given an antibiotic immediately after birth. The reason is that many years ago, before antibiotics, women who unknowingly had gonorrhea would pass the infection to their babies, giving the newborns terrible eye infections that could cause blindness.
So 4 million babies born in the United States every year are given antibiotic eye-drops to prevent an illness that occurs very rarely. The dose is low but is likely affecting the composition of the infant’s resident microbes just when the founding populations are developing. We should be able to develop a better way to screen, so we can target those babies at the highest risk, perhaps a few hundred among the millions of births a year.
Although babies are born into a world replete with diverse bacteria, the ones that colonize them are not accidental. These first microbes colonizing the newborn begin a dynamic process. We are born with innate immunity, a collection of proteins, cells, detergents, and junctions that guard our surfaces based on recognition of structures that are widely shared among classes of microbes. In contrast, we must develop adaptive immunity that will clearly distinguish self from non-self. Our early-life microbes are the first teachers in this process, instructing the developing immune system about what is dangerous and what is not.
In our first three years of life, a great diversity of microbes self-organizes into a life-support system with the complexity of the adult microbiota. This critical period lays the foundation for all the biological processes that unfold in our childhood, adolescence, adulthood, and old age—unless something comes along to disrupt it.
Adapted and excerpted from Missing Microbes: How the Overuse of Antibiotics Is Fueling Our Modern Plagues. Copyright 2014 Martin J. Blaser, M.D. Reprinted with permission from Henry Holt and Company.